Decapod crustacean assemblages on trawlable grounds in the northern Alboran Sea and Gulf of Vera

INTRODUCTION

The Alboran Sea, located in the westernmost part of the Mediterranean Sea, is a transitional area between the Atlantic Ocean and the Mediterranean Sea that has been reported as a self-standing ecoregion harbouring a large marine biodiversity and a wide variety of habitats (Spalding et al. 2007Spalding M., Fox H., Allen G., et al. 2007. Marine Ecoregions of the World: A Bioregionalization of Coastal and Shelf Areas. BioScience. 57: 573-583. https://doi.org/10.1641/B570707 , Rueda et al. 2021Rueda J.L., Gofas S., Aguilar R., et al. 2021. Chapter 9: Benthic fauna of littoral and deep-sea habitats of the Alboran Sea: A hotspot of biodiversity. In: Báez J.C., Vázquez J.T., et al. (eds), Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 285-358. https://doi.org/10.1007/978-3-030-65516-7_9 , Templado et al. 2021Templado J., Luque A.A., Moreno D., et al. 2021. Chapter 10: Invertebrates: The realm of diversity. In: Báez J.C., Vázquez J.T., Camiñas J.A., Malouli M. (eds), Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 359-430. https://doi.org/10.1007/978-3-030-65516-7_10 ). Because of its distinctive geomorphological and oceanographical features, the Alboran Sea has been identified as a specific biogeographical sector for several marine groups (Real et al. 2021Real R., Gofas S., Altamarino M., et al. 2021. Chapter 11: Biogeographical and Macroecological context of the Alboran Sea. In: Báez J.C., Vázquez J.T., Camiñas J.A., Malouli M. (eds), Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 431-457. https://doi.org/10.1007/978-3-030-65516-7_11 ), including demersal fish (Gaertner et al. 2005Gaertner J.C., Bertrand J.A, Gil de Sola L., et al. 2005. Large spatial scale variation of demersal fish assemblage structure on the continental shelf of the NW Mediterranean Sea. Mar. Ecol. Prog. Ser. 297: 245-257. https://doi.org/10.3354/meps297245 , González et al. 2021González M., García-Ruiz C., García J., et al. 2021. Chapter: 18: Demersal Resources. In: Báez J.C., Vázquez J.T., et al. (eds), Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 589-628. https://doi.org/10.1007/978-3-030-65516-7_18 ), molluscs (Gofas et al. 2011Gofas S., Moreno D., Salas C. 2011. Moluscos marinos de Andalucía. Volúmenes I y II. Servicio de Publicaciones e Intercambio Científico, Universidad de Málaga, Málaga, 798 pp., Ciércoles et al. 2018Ciércoles C., García-Ruiz C., González M., et al. 2018. Molluscs collected with otter trawl in the northern Alboran Sea: main assemblages, spatial distribution and environmental linkage. Mediterr. Mar. Sci. 19: 209-222. https://doi.org/10.12681/mms.2124 ) and crustaceans (Abelló et al. 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 ).

Crustaceans are one of the most morphologically diverse taxonomic groups of the aquatic ecosystems, where they are one of the top dominant groups (Martin and Davis 2001Martin J.W., Davis G.E. 2001. An updated classification of the Recent Crustacea. Natural History Museum of Los Angeles County, Los Angeles, 124 pp.). Within the crustaceans, the order Decapoda constitutes a dominant component of Mediterranean benthic and demersal communities of both the continental shelf and slope (Maynou and Cartes 2000Maynou F., Cartes E.J. 2000. Community structure of bathyal decapods crustaceans off south-west Balearic Islands (western Mediterranean): seasonality and regional patterns in zonation. J. Mar. Biol. Ass. U.K. 80: 789-798. https://doi.org/10.1017/S0025315400002769 , Guijarro 2012Guijarro B. 2012. Population dynamics and assessment of exploited deep water decapods off Balearic Islands (western Mediterranean): from single to multi-species approach. Ph. D. thesis, Balearic Islands Univ. Balearic Islands, 257 pp. https://doi.org/10.1007/s10750-011-0670-z ). Their relative importance in the Mediterranean Sea has been hypothesized because of their very high competitive trophic strategy (Cartes and Sardà 1992Cartes J.E., Sardà F. 1992. Abundance and diversity of decapods crustaceans in the deep-Catalan Sea (Western Mediterranean). J. Nat. Hist. 26: 1305-1323. https://doi.org/10.1080/00222939200770741 , Maynou and Cartes 2000Maynou F., Cartes E.J. 2000. Community structure of bathyal decapods crustaceans off south-west Balearic Islands (western Mediterranean): seasonality and regional patterns in zonation. J. Mar. Biol. Ass. U.K. 80: 789-798. https://doi.org/10.1017/S0025315400002769 ). Moreover, decapods are a key taxon linking lower and higher trophic levels (Cartes 1998Cartes J.E. 1998. Feeding strategies and partition of food resources in Deep-Water Decapod Crustacean (400-2300 m). J. Mar. Biol. Ass. U.K. 78: 509-524. https://doi.org/10.1017/S002531540004159X , Fanelli 2007Fanelli E., Colloca F., Ardizzone G. 2007. Decapod crustacean assemblages off the West coast of central Italy (western Mediterranean). Sci. Mar. 71: 19-28. https://doi.org/10.3989/scimar.2007.71n119 ). Several decapod species are of commercial interest and form an important component of the catches of the bottom trawl fishery in the Alboran Sea and the Gulf of Vera. In fact, some decapod species, such as the deep-water rose shrimp, Parapenaeus longirostris, the Norway lobster, Nephrops norvegicus, and the red shrimp Aristeus antennatus are economically valuable target species in demersal fisheries, so their populations are regularly assessed in the Alboran Sea (González et al. 2021González M., García-Ruiz C., García J., et al. 2021. Chapter: 18: Demersal Resources. In: Báez J.C., Vázquez J.T., et al. (eds), Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 589-628. https://doi.org/10.1007/978-3-030-65516-7_18 ), as well as in other parts of the Mediterranean Sea (Guijarro 2012Guijarro B. 2012. Population dynamics and assessment of exploited deep water decapods off Balearic Islands (western Mediterranean): from single to multi-species approach. Ph. D. thesis, Balearic Islands Univ. Balearic Islands, 257 pp. https://doi.org/10.1007/s10750-011-0670-z ; Regulation (EU) 2019/1022). Knowledge of the distribution and abundance of species along environmental gradients has traditionally been important to characterize and understand the role of biological communities in aquatic systems (Wenner and Boesch 1979Wenner E. L., Boesch D. F. 1979. Distribution patterns of epibenthic decapod Crustacea along the shelf-slope coenocline, middle Atlantic Bight, U.S.A. Bull. Biol. Soc. Wash. 3: 106-133. https://doi.org/10.1175/1520-0485(1991)021<0811:MDAVMI>2.0.CO;2 ). Studies of biological communities are also essential tools for understanding the dynamics of exploited species from an ecosystem point of view, which is a key element in considering separate management units (Abelló et al. 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 ). Additionally, species-specific studies on decapod species have revealed geographical variability patterns throughout the Mediterranean Sea, reflecting the importance of studies at a small-scale geographical level. This approach has been shown to be more efficient for the management of certain species in contrast to large regional approaches (Gaertner et al. 2005Gaertner J.C., Bertrand J.A, Gil de Sola L., et al. 2005. Large spatial scale variation of demersal fish assemblage structure on the continental shelf of the NW Mediterranean Sea. Mar. Ecol. Prog. Ser. 297: 245-257. https://doi.org/10.3354/meps297245 , Guijarro et al. 2019Guijarro B., Bitetto I., D’Onghia G., et al. 2019. Spatial and temporal patterns in the Mediterranean populations of Aristaeomorpha foliacea and Aristeus antennatus (Crustacea: Decapoda: Aristeidae) based on the MEDITS surveys. Sci. Mar. 83: 57-70. https://doi.org/10.3989/scimar.05012.04A ) and it is particularly important for scientifically sustaining spatial management. The Alboran Sea, together with the Gulf of Vera, can be considered a transition zone between the Mediterranean and Atlantic biota of crustaceans, since it also constitutes a semipermeable barrier for genetic population exchanges between the Mediterranean Sea and the Atlantic Ocean (Abelló et al. 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 , Mateo-Ramírez et al. 2015Mateo-Ramírez Á., Farias C., Gallardo Roldán H., et al. 2015. Asociaciones de decápodos de fondos blandos circalitorales y batiales del mar de Alborán. In: Díaz del Rio V., Bárcenas P., et al. (eds), Volumen de Comunicaciones presentadas en el VII Simposio sobre el Margen Ibérico Atlántico. Sia Graf, Málaga, pp. 433-436., Pascual et al. 2016Pascual M., Palero F., García-Merchán VH., et al. 2016. Temporal and spatial genetic differentiation in the crab Liocarcinus depurator across the Atlantic-Mediterranean transition. Sci. Rep. 6: 29892: 1-10. https://doi.org/10.1038/srep29892 ).

Several studies on decapod assemblages have been carried out in different habitats of the Alboran Sea, particularly those of the infralittoral zone (soft bottoms, García Muñoz et al. 2008García Muñoz J.E., Manjón Cabeza M.E., García Raso J.E. 2008. Decapod crustacean assemblages from littoral bottoms of the Alborán Sea (Spain, west Mediterranean Sea): spatial and temporal variability. Sci. Mar. 72: 437-449. https://doi.org/10.3989/scimar.2008.72n3437 ; seagrass meadows, García-Raso 1990García Raso J.E. 1990. Study of a Crustacea Decapoda Taxocoenosis of Posidonia beds from the Southeast of Spain. Marine Ecology, PSZN 11: 309-326. https://doi.org/10.1111/j.1439-0485.1990.tb00386.x , García Raso et al. 2006García Raso J.E., Martín M.J., Díaz V., et al. 2006. Diel and seasonal changes in the structure of a Decapod (Crustacea: Decapoda) community of Cymodocea nodosa from Southeastern Spain (West Mediterranean Sea). Hydrobiologia 557: 59-68. https://doi.org/10.1007/1-4020-4756-8_8 , Mateo-Ramírez et al. 2016Mateo-Ramírez Á., Urra J., Marina Ureña P., et al. 2016. Crustacean decapod assemblages associated with fragmented Posidonia oceanica meadows in the Alboran Sea (Western Mediterranean Sea): composition, temporal dynamics and influence of meadow structure. Mar. Ecol. 37: 344-358. https://doi.org/10.1111/maec.12284 ; macroalgal communities, Mateo-Ramírez et al. 2018Mateo-Ramírez Á., Urra J., Rueda J.L., et al. 2018. Decapod assemblages associated with shallow macroalgal communities in the northwestern Alboran Sea: Microhabitat use and temporal variability. J. Sea Res. 135: 84-94. https://doi.org/10.1016/j.seares.2018.02.009 ). However, despite their ecological and economical interest, few studies of decapod assemblages in circalittoral and bathyal soft bottoms have been carried out in the Alboran Sea using beam-trawl samples (Mateo-Ramírez et al. 2015Mateo-Ramírez Á., Farias C., Gallardo Roldán H., et al. 2015. Asociaciones de decápodos de fondos blandos circalitorales y batiales del mar de Alborán. In: Díaz del Rio V., Bárcenas P., et al. (eds), Volumen de Comunicaciones presentadas en el VII Simposio sobre el Margen Ibérico Atlántico. Sia Graf, Málaga, pp. 433-436.) or including the Alboran Sea as part of studies with a wider scope covering the Spanish Mediterranean waters (Abelló et al. 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 ).

The aims of this study were to (1) update faunistic inventories of decapod crustacean species in the Alboran Sea and the adjacent Gulf of Vera; (2) identify and characterize the main decapod assemblages; (3) analyse significant differences between assemblages in the ecological indices considered as community descriptors (decapod abundance, species richness, Pielou’s evenness and the Shannon-Wiener diversity index) in order to study the spatial and temporal changes of the composition and structure of the decapod assemblages; and (4) model spatio-temporal trends of ecological indices in terms of potential environmental driving.

MATERIALS AND METHODS

Study area

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The study area covers approximate 12753 km² and encompasses the northern Alboran Sea and Gulf of Vera, from Punta Europa (Strait of Gibraltar) to Cabo de Palos (Cartagena), including also the Alboran Island (Fig. 1). The main hydrological characteristics of this area are the mixture of Atlantic and Mediterranean water masses with (1) Atlantic surficial water masses entering the Mediterranean Sea and extending from the surface to 200 m depth; (2) Intermediate Levantine water masses from the Mediterranean Sea, flowing towards the Atlantic Ocean and usually extending from 200 to 600 m depth; and (3) deep water masses extending below the Levantine water masses to the sea bottom (Parrilla et al. 1986Parrilla G., Kinder T., Preller R. 1986. Deep and Intermediate Mediterranean Water in the western Alboran Sea. Deep Sea Res. Part A. Ocenographic Research Papers 33: 55-88. https://doi.org/10.1016/0198-0149(86)90108-1 , Vargas-Yáñez et al. 2017Vargas-Yáñez M., García-Martínez M.C., Moya F., et al. 2017. Updating temperature and salinity mean values and trend in the Western Mediterranean: The RADMED Project. Prog. Oceanogr. 157: 27-46. https://doi.org/10.1016/j.pocean.2017.09.004 ). The different physico-chemical characteristics of these water masses, together with the density contrast and the geomorphology of the Alboran basin, are responsible for the complex hydrodynamic processes that take place in the area, along with the presence of the Alboran Gyre and nutrient-rich coastal upwellings (Tintoré et al. 1991Tintoré J., Gomis D., Alonso S. 1991. Mesoscale Dynamics and Vertical Motion in the Alborán Sea. J. Phys. Oceanogr. 21: 811-823. https://doi.org/10.1175/1520-0485(1991)021<0811:MDAVMI>2.0.CO;2 , Vargas-Yáñez et al. 2010Vargas-Yáñez M., García-Martínez M.C., Moya F., et al. 2010. Cambio climático en el Mediterráneo español. Instituto Español de Oceanografía, Ministerio de Ciencia e Innovación, Madrid, 176 pp., 2021Vargas-Yáñez M., García-Martínez M.C., Moya F., et al. 2021. Chapter 4: The Oceanographic and Climatic Context. In: Báez J.C., Vázquez J.T., et al. eds), Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 85-109. https://doi.org/10.1007/978-3-030-65516-7_4 ). The seafloor of the study area has a high geomorphological complexity with a wide variety of reliefs, such as depressions, banks, ridges and canyons (Parrilla and Kinder 1987Parrilla G., Kinder T. 1987. The Physical Oceanography of the Alboran Sea. NORDA Report 184, 26 pp., Ercilla et al. 1992Ercilla G., Alonso B., Baraza J. 1992. Sedimentary evolution of the northwestern Alboran Sea during the Quaternary. Geo-Mar. Let. 12: 144-149. https://doi.org/10.1007/BF02084925 , 2021Ercilla G., Vázquez J.T., Alonso B., et al. 2021. Chapter 6: Seafloor Morphology and Processes in the Alboran Sea. In: Báez J.C., Vázquez J.T., et al. (eds), Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 157-205. https://doi.org/10.1007/978-3-030-65516-7_6 ). The northern Alboran Sea and the Gulf of Vera are both characterized by a very narrow continental shelf with alternating predominance of sands and muds, while the continental slope is mainly composed of very fine sediments (Rey and Medialdea 1989Rey J., Medialdea T. 1989. Los sedimentos cuaternarios superficiales del Margen Continental Español. Publicaciones especiales Instituto Español de Oceanografía. 3, Madrid, 36 pp., Ercilla et al. 2021Ercilla G., Vázquez J.T., Alonso B., et al. 2021. Chapter 6: Seafloor Morphology and Processes in the Alboran Sea. In: Báez J.C., Vázquez J.T., et al. (eds), Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 157-205. https://doi.org/10.1007/978-3-030-65516-7_6 ). In addition, the Alboran Sea, together with the Gulf of Lion and the mouth of different rivers (e.g. the Ebro River on the northeastern Spanish Mediterranean coast), is one of the areas with the highest primary production in the western Mediterranean (Vargas-Yáñez et al. 2010Vargas-Yáñez M., García-Martínez M.C., Moya F., et al. 2010. Cambio climático en el Mediterráneo español. Instituto Español de Oceanografía, Ministerio de Ciencia e Innovación, Madrid, 176 pp.). This is due to several processes (e.g. nutrient flows from rivers and nutrient-rich coastal upwelling) that favour the injection of nutrients into the photophilous zone of the water column (Báez et al. 2021Báez J.C., Vázquez J.T., Camiñas J.A., Idrissi M.M (eds). 2021. Alboran Sea -Ecosystems and Marine Resources. Springer Nature Switzerland AG, 956 pp. https://doi.org/10.1007/978-3-030-65516-7 ). The Gulf of Vera is also a strategic location in the western Mediterranean since it is adjacent to the Almería-Oran front, which forms a semi-permanent hydrographic barrier and a transition zone between the Alboran Sea (an area with greater Atlantic water influence) and the rest of the western Mediterranean basin (Tintoré et al. 1988Tintoré J., La Violette P.E., Blade I., Cruzado A. 1988. A study of an Intense Density Front in the Eastern Alboran Sea: The Almeria-Oran Front. J. Phys. Oceanogr. 18: 1384-1397. https://doi.org/10.1175/1520-0485(1988)018<1384:ASOAID>2.0.CO;2 , Millot 1999Millot C. 1999. Circulation in the Western Mediterranean Sea. J. Mar. Syst. 20: 423-442. https://doi.org/10.1016/S0924-7963(98)00078-5 ). The meridional sector of the Alboran Sea is characterized by the presence of an old volcanic ridge oriented SW-NE, on which Alboran Island is located (Vázquez 2005Vázquez J.T. 2005. El margen continental del Mar de Alborán. In: Martín-Serrano A. (ed.), Mapa Geomorfológico de España y del margen continental. Instituto Geológico y Minero de España, pp. 191-198.). This island is affected by the circulation of the water masses present in the Alboran basin and has been described as an anticyclonic area located between two geostrophic gyres of the incoming Atlantic surface water. These peculiar hydrological characteristics result in the singularity and extraordinary biodiversity of the benthic communities of the Alboran Island (Gofas et al. 2014Gofas S., Goutayer J., Luque Á.A., et al. 2014. Espacio Marino de Alborán. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, 129 pp.), as well as of the Alboran Sea (Rueda et al. 2021Rueda J.L., Gofas S., Aguilar R., et al. 2021. Chapter 9: Benthic fauna of littoral and deep-sea habitats of the Alboran Sea: A hotspot of biodiversity. In: Báez J.C., Vázquez J.T., et al. (eds), Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 285-358. https://doi.org/10.1007/978-3-030-65516-7_9 ). This high diversity promoted the protection of the Alboran Island and its surrounding bottoms through protection measures such as a Marine and Fishing Reserve, a Site of Community Importance and a Specially Protected Area of Mediterranean Importance (Mateo-Ramírez et al. 2021Mateo-Ramírez, Á., Marina, P., Moreno, D., et al. 2021. Marine Protected Areas and Key Biodiversity Areas of the Alboran Sea and Adjacent Areas. Alboran Sea - Ecosyst. Mar. Resour. 819-923. https://doi.org/10.1007/978-3-030-65516-7_25 ).

Fig. 1.  - Map of the study area showing the sampling stations (black points) used during MEDITS surveys (2012 to 2018) and the sectors considered.

RESULTS

Affinity between samples

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Cluster and nMDS analyses performed on abundance data revealed four groups of samples (interpreted as different decapod assemblages) that were mainly related to depth: the first group corresponded to an inner/shallow shelf (IS) assemblage at 30 to 100 m depth; the second group corresponded to an outer shelf (OS) assemblage at 101 to 200 m depth; the third corresponded to an upper slope (US) assemblage at 201 to 500 m depth and the fourth corresponded to a middle slope (MS) assemblage to 501 to 800 m depth (Fig. 2). SIMPER analyses showed that the decapods D. arrosor, L. depurator, M. longipes and P. prideaux characterized the IS assemblage, whereas P. heterocarpus, D. arrosor, P. prideaux and M. longipes characterized the OS assemblage. The US assemblage was characterized by P. heterocarpus, P. longirostris, S. membranacea and D. arrosor, and the MS assemblage was characterized by P. martia, P. acanthonotus, Pagurus alatus and Sergia robusta (Table 3). The largest differences were observed between the shelf assemblages (IS and OS) and the MS assemblage (av. diss. >96%). These differences were mainly due to the higher abundance of D. arrosor and L. depurator in the IS assemblage, P. heterocarpus and P. prideaux in the OS assemblage, P. longirostris and S. membranacea in the US assemblage, and P. martia, P. acanthonotus, P. alatus and S. robusta in the MS assemblage.

Fig. 2.  - Results of the nMDS analysis performed on samples using the Bray-Curtis similarity index based on decapod abundance data (square-root transformed) during MEDITS surveys (2012-2018). IS, inner shelf assemblage; OS, outer shelf assemblage; US, upper slope assemblage; MS, middle slope assemblage.

Table 3.  - Results of the SIMPER analyses displaying the species contribution to the similarity of each detected decapod assemblage using multivariate methods. Av. Abund, average abundance; Contrib%, percentage contribution to the similarity; Cum%, cumulative percentage of species contribution, up to ca. 90%.

Inner shelf: 30-100 m Average similarity: 33.11					Outer shelf: 101-200 m Average similarity: 29.64
species	Av.Abund	Contrib%	Cum%		species	Av.Abund	Contrib%	Cum%
Dardanus arrosor	25.1	49.53	49.53		Plesionika heterocarpus	132.44	41.88	41.88
Liocarcinus depurator	20.16	20.35	69.88		Dardanus arrosor	24.55	28.31	70.19
Macropodia longipes	10.93	14.97	84.85		Pagurus prideaux	19.84	12.37	82.56
Pagurus prideaux	10.24	6.6	91.45		Macropodia longipes	8.29	8.26	90.82
Upper Slope: 201-500 m average similarity: 32.49					Middle Slope: 501-800 m average similarity: 51.81
species	Av.Abund	Contrib%	Cum%		species	Av.Abund	Contrib%	Cum%
Plesionika heterocarpus	48.92	27.53	27.53		Plesionika martia	26.28	1.79	28.11
Parapenaeus longirostris	18.81	15.15	42.68		Plesionika acanthonotus	15.65	1.81	46.04
Solenocera membranacea	12.85	9.25	51.92		Pagurus alatus	11.27	1.68	57.8
Dardanus arrosor	8.2	8.43	60.35		Sergia robusta	10.58	1.57	68.22
Plesionika martia	12.66	6.49	66.84		Polycheles typhlops	7.96	1.31	76.72
Pasiphaea sivado	21.03	6.43	73.27		Pasiphaea multidentata	7.02	7.02	83.74
Nephrops norvegicus	5.83	3.99	77.26		Aristeus antennatus	8.45	3.57	87.32
Macropodia longipes	4.87	3.64	80.89		Rochinia carpenteri	2.76	1.97	89.29
Plesionika gigliolii	7.92	3.38	84.27		Solenocera membranacea	3.39	1.91	91.19
Macropipus tuberculatus	3.56	1.72	85.99
Liocarcinus depurator	3.97	1.71	87.7
Alpheus glaber	3.28	1.5	89.2
Processa canaliculata	2.78	1.48	90.69

The PERMANOVA test revealed significant differences between geographical sectors of the study area (Table 4). Pairwise comparisons after PERMANOVA analyses showed that: significant differences for the OS assemblage were detected between the Alboran Island-northern Alboran Sea and Alboran Island-Gulf of Vera sectors (p<0.05), while significant differences for the US and the MS assemblages were detected between the three sectors (p<0.05 in all cases). As mentioned previously, this analysis was not carried out for the IS assemblage since this bathymetric stratum could not be sampled in Alboran Island.

Table 4.  - Results of the PERMANOVA analyses testing differences between three of the four detected assemblages (OS, US, MS) and the three considered sectors (northern Alboran Sea, Gulf of Vera and Alboran Island).

Source	df	MS	Pseudo-F	p
Assemblages (AS)	2	98888	56.56	0.001
Sector (SE)	2	22716	12.99	0.001
ASxSE**	4	10419	5.95	0.001
Res	292	1748.4
Total	300

Ecological indices

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Significant differences were found between assemblages for all ecological indices tested. With regard to the mean abundance data, the significant maximum values were for the OS and US assemblages, while the minimum ones were detected for the MS assemblage, followed by the IS assemblage (Kruskal-Wallis test: c²=92.6; p<0.01) (Fig. 3A). Mean species richness showed significant maximum values in the US and MS assemblages and minimum ones in the IS assemblage (Kruskal-Wallis test: c²=187.6; p<0.01) (Fig. 3B). The mean Shannon-Wiener diversity index displayed significant maximum values in the deepest assemblages (US and MS) and minimum ones in the OS assemblage (Kruskal-Wallis test: c²=190.5; p<0.01) (Fig. 3C). The mean Pielou’s evenness index displayed significant maximum values in the MS and IS assemblages and minimum ones in the OS assemblage (Kruskal-Wallis test: c²=58.80; p<0.01) (Fig. 3D).

Fig. 3.  - Mean values of the ecological indices: (A) abundance (ind. km^-2); (B) species richness; (C) Shannon-Wiener diversity index; (D) Pielou’s evenness index for each decapod assemblages detected in multivariate analyses. Mean±SE. Letters above error bars display the results of Kruskal-Wallis pairwise test: different letters distinguish significantly different means at p<0.01.

GAM models for testing spatio-temporal variability of ecological indices

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For all ecological indices, GAM analyses showed a statistically significant effect of depth and the latitude-longitude bivariate smoother (hereafter referred to as the geographical effect). The best models included depth and the geographical effect, together with year as a factor, and explained 46.2% of the deviance (DE) for abundance, 64.6% for species richness, 49.6% for Shannon-Wiener diversity index and 34.4% for Pielou’s evenness index (Table 5) (Appendix 1 and 2). No significant effect was found for the selected environmental variables of this study, including the NAO index. The depth influence was related to (1) a peak of abundance at 200 m with a progressive decrease with depth (Fig. 4A); (2) a continuous increase in species richness with a peak at 400 m followed by a slight decrease (Fig. 4B); and (3) a minimum value at 200 m with two peaks at 400 and 600 m depth for the Shannon-Wiener diversity and Pielou’s evenness index (Fig. 4C, D). The geographical effect was related to (1) maximum abundance values in the westernmost part of the study area and at Cabo de Gata (Fig. 4A); (2) maximum species richness in the westernmost and easternmost parts of the study area (Fig. 4B); (3) maximum Shannon-Wiener diversity index values in the Gulf of Vera (Fig. 4C); and (4) a similar and high Pielou’s evenness index throughout the study area (Fig. 4D). Regarding the factor “year”, abundance and species richness showed similar temporal patterns with a slight trend to decrease over successive years and with maximum values in 2012 and 2018 (Fig. 4A, B). For the Shannon-Wiener diversity index, the highest value was recorded in 2012, but no clear temporal trend was detected, as observed for Pielou’s evenness index, which showed similar values throughout the time series (Fig. 4C, D) (Appendices 1 and 2).

Table 5.  - Results of generalized additive models (GAM) for the ecological indices analysed. N, abundance (log transformed); S, species richness; H’, Shannon-Wiener diversity index; J’, Pielou’s evenness index. Lat and long, latitude and longitude for geographical effect; Chl a, chlorophyll a concentration (mg·m^-3); SBT, sea bottom temperature; SBS, sea bottom salinity. Values refer to the edf (degrees of freedom). DE(%), percentage of variance explained. ns, Non-significant effect. Asterisks denote significance levels: ***, p<0.001; **, p<0.01; *, p<0.05.

Model	Depth	Lat and long	NAO	Chl a	NO3	SBT	SBS	DE(%)
N	5.40**	23.38***	ns	ns	ns	ns	ns	46.2
S	5.76***	18.50***	ns	ns	ns	ns	ns	64.6
H’	8.01***	19.93**	ns	ns	ns	ns	ns	49.6
J’	6.48***	20.81**	ns	ns	ns	ns	ns	34.4

Fig. 4.  - Partial effects of year (left column), depth (middle column), and geographic distribution (combination of longitude and latitude) (right column) for (A) abundance (ind. km^-2) (log-transformed), (B) species richness, (C) Shannon-Wiener diversity index and (D) Pielou’s evenness index. The colour gradient of the geographical effect ranges from low values (darker-blue colours) to high values (lighter-green colours).

DISCUSSION

The present study reports a high number of decapod species on circalittoral and bathyal soft bottoms of the northern Alboran Sea, including Alboran Island and the Gulf of Vera, and increases the number of previously recorded species for these sedimentary habitats (15 additional species to those reported by Abelló et al. 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 ). Nevertheless, all the species detected in the present study were previously listed in the Alboran Sea by Marco-Herrero et al. (2017) and García-Raso et al. (2018)García Raso J.E., García Muñoz J.E., Mateo-Ramírez A., et al. 2018. Decapod crustaceans Eucalliacidae in chemoautotrophic bathyal bottoms of the Gulf of Cadiz (Atlantic Ocean), environmental characteristics and associated communities. J. Mar. Biol. Assoc. U.K. 99: 437-444. https://doi.org/10.1017/S0025315418000280 in a bibliographic compilation of marine decapod crustaceans from the Iberian Peninsula. A high decapod richness for the Alboran Sea was already reported by García Muñoz et al. (2008)García Muñoz J.E., Manjón Cabeza M.E., García Raso J.E. 2008. Decapod crustacean assemblages from littoral bottoms of the Alborán Sea (Spain, west Mediterranean Sea): spatial and temporal variability. Sci. Mar. 72: 437-449. https://doi.org/10.3989/scimar.2008.72n3437 in infralittoral sedimentary habitats, and this was related to a high diversity of bottom and habitat types and the confluence of Atlantic and Mediterranean waters and organisms. Abelló et al. (2002)Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 highlighted that the exceptional and highly diverse decapod assemblages of the shelf and slope of the northern Alboran Sea, with a biogeographical boundary around Cabo de Palos, made this area very different from other western Mediterranean areas.

Comparing the geographical sectors of the study area, the highest number of species was detected in the northern Alboran Sea (86 spp.), whereas the lowest number was found at Alboran Island and in the Gulf of Vera (55 and 54 spp., respectively). It is important here to reiterate that no sampling could be carried out at depths shallower than 100 m around Alboran Island because it is a Marine and Fishing Reserve and bottom trawling is not allowed because of the occurrence of vulnerable marine ecosystems (Mateo-Ramírez et al. 2021Mateo-Ramírez, Á., Marina, P., Moreno, D., et al. 2021. Marine Protected Areas and Key Biodiversity Areas of the Alboran Sea and Adjacent Areas. Alboran Sea - Ecosyst. Mar. Resour. 819-923. https://doi.org/10.1007/978-3-030-65516-7_25 ). Species with Atlantic affinities, most of them with a low frequency of occurrence (F<0.73%) (such as P. henslowii, Ergasticus clouei, and Pagurus mbizi), were recorded in the northern Alboran Sea and/or Alboran Island sectors but not in the Gulf of Vera sector, in agreement with Abelló et al. (2002)Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 . This could be due to the effect of the semi-permanent Almeria-Oran oceanographic front that acts as an effective barrier for gene flow and/or species dispersion for these species, as has also been detected for some other decapod species (García Raso et al. 2014García Raso J.E., Salmeron F., Baro J., et al. 2014. The tropical African hermit crab Pagurus mbizi (Crustacea, Decapoda, Paguridae) in the Western Mediterranean Sea: a new alien species or filling gaps in the knowledge of the distribution?. Meditter. Mar. Sci. 15:172-178 https://doi.org/10.12681/mms.530 , García Lafuente et al. 2021García Lafuente J., Sanchez-Garrido J.C., Garcia A., et al. 2021. Chapter 12: Biophysical Processes Determining the Connectivity of the Alboran Sea Fish Populations. In: Báez J.C., Vázquez JT., et al. (eds). Alboran Sea - Ecosystems and Marine Resources. Springer Nature Switzerland AG, pp. 459-487. https://doi.org/10.1007/978-3-030-65516-7_12 ). It is worth mentioning the occurrence of the subtropical Atlantic hermit crab P. mbizi (Forest 1955). It was initially reported in 2014 in the westernmost sector of the northern Alboran Sea (an exclusive occurrence in European waters and the Mediterranean Sea) by García Raso et al. (2014)García Raso J.E., Salmeron F., Baro J., et al. 2014. The tropical African hermit crab Pagurus mbizi (Crustacea, Decapoda, Paguridae) in the Western Mediterranean Sea: a new alien species or filling gaps in the knowledge of the distribution?. Meditter. Mar. Sci. 15:172-178 https://doi.org/10.12681/mms.530 in a depth range of 50 to 150 m. In the present study, specimens of P. mbizi were collected in the central and eastern parts of the northern Alboran Sea over a wider bathymetric range (50-361 m), showing a similar depth range to that recorded in Atlantic waters (30 -650 m) (Forest 1961Forest J. 1961. Pagurides de l’Afrique occidentale. Atlantide Report, 6: 203-250.). However, P. mbizi was absent in the Gulf of Vera, so its expansion is so far restricted to the Alboran Sea. On the other hand, the crab Scyramathia carpenteri (previously known as Rochinia carpenteri) was first recorded in the northern Alboran Sea sector (Abelló et al. 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 ), but the present study provides records for the Gulf of Vera sector, thus suggesting a possible expansion to other western Mediterranean areas. The presence and, in some cases, potential eastward expansion of typical Atlantic species (e.g. S. carpenteri) and African species (e.g. P. mbizi) through the Alboran Sea could be a result of climate change effects, favouring a northwards expansion of thermophilic Atlantic species along the Atlantic coasts and into the Mediterranean Sea (i.e. meridionalization) (García Raso et al. 2014García Raso J.E., Salmeron F., Baro J., et al. 2014. The tropical African hermit crab Pagurus mbizi (Crustacea, Decapoda, Paguridae) in the Western Mediterranean Sea: a new alien species or filling gaps in the knowledge of the distribution?. Meditter. Mar. Sci. 15:172-178 https://doi.org/10.12681/mms.530 , 2018García Raso J.E., Cuesta J.A., Abelló P., Macpherson E. 2018. Updating changes in the Iberian decapod crustacean fauna (excluding crabs) after 50 years. Sci. Mar. 82: 207-229. https://doi.org/10.3989/scimar.04831.04A ), once they manage to surpass the colder waters of the Alboran Sea.

Marine species distribution is generally related to dynamic environmental variables such as temperature and other variables such as food availability (Snelgrove and Butman 1994Snelgrove P.V., Butman C.A. 1994. Animal-sediment relationships revisited: Causes versus effect. Oceanogr.Mar. Biol. 32: 111-177., Cartes et al. 2004Cartes J.E., Maynou F., Moranta J., et al. 2004. Patterns of bathymetric distribution among deep-sea fauna at local spatial scale: comparison of mainland vs. insular areas. Prog. Oceanogr. 60: 29-45. https://doi.org/10.1016/j.pocean.2004.02.001 , Martins et al. 2014Martins R., Sampaio L., Quintino V., Rodrigues A.M. 2014. Diversity, distribution and ecology of benthic molluscan communities on the Portuguese continental shelf. J. Sea Res. 93: 75-89. https://doi.org/10.1016/j.seares.2013.11.006 ), but it is also related to structural properties such as depth and the substrate type of the seabed. As in previous studies (Cartes and Sardà 1993Cartes J.E., Sardà F. 1993. Zonation of deep-sea decapod fauna in the Catalan Sea (Western Mediterranean). Mar. Ecol. Prog. Ser. 94: 27-34. https://doi.org/10.3354/meps094027 , Follesa et al. 2009Follesa M.C., Porcu C., Gastoni A., et al. 2009. Community structure of bathyal decapod crustaceans off South-Eastern Sardinian deep-waters (Central-Western Mediterraenan). Mar. Ecol. 30: 188-199. https://doi.org/10.1111/j.1439-0485.2009.00323.x , Deval et al. 2017Deval M., Yilmaz S., Kapiris K. 2017. Spatio Temporal Variations in Decapod Crustacean Assemblages of Bathyal Ground in the Antalya Bay (Eastern Mediterranean). Turkish J. Fish. Aquat. Sci. 17: 967-979. https://doi.org/10.4194/1303-2712-v17_5_12 , among others), depth was the main structuring factor for decapod crustacean distribution in the present study, probably because of a combination of other depth-related factors such as light, temperature and food availability (Cartes et al. 2004Cartes J.E., Maynou F., Moranta J., et al. 2004. Patterns of bathymetric distribution among deep-sea fauna at local spatial scale: comparison of mainland vs. insular areas. Prog. Oceanogr. 60: 29-45. https://doi.org/10.1016/j.pocean.2004.02.001 ). In the present study, four decapod assemblages were detected in relation to depth, in agreement with previous studies on the northern Alboran Sea (Mateo-Ramírez et al. 2015Mateo-Ramírez Á., Farias C., Gallardo Roldán H., et al. 2015. Asociaciones de decápodos de fondos blandos circalitorales y batiales del mar de Alborán. In: Díaz del Rio V., Bárcenas P., et al. (eds), Volumen de Comunicaciones presentadas en el VII Simposio sobre el Margen Ibérico Atlántico. Sia Graf, Málaga, pp. 433-436.), adjacent Mediterranean areas (Abelló et al. 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 , García-Rodríguez et al. 2011García Rodríguez M., Abelló P., Fernández A., Esteban A. 2011. Demersal Assemblages on the Soft Bottoms off the Catalan-Levante Coast of the Spanish Mediterranean. J. Mar. Biol. 2011: 1-16. https://doi.org/10.1155/2011/976396 , Deval et al. 2017Deval M., Yilmaz S., Kapiris K. 2017. Spatio Temporal Variations in Decapod Crustacean Assemblages of Bathyal Ground in the Antalya Bay (Eastern Mediterranean). Turkish J. Fish. Aquat. Sci. 17: 967-979. https://doi.org/10.4194/1303-2712-v17_5_12 , among others) and adjacent Atlantic waters (López de la Rosa 1997López de la Rosa I. 1997. Crustáceos decápodos capturados durante las campañas del IEO ARSA 0393 y ARSA 1093 en el golfo de Cádiz: distribución batimétrica. Publ. Espec. Inst. Esp. Oceanogr. 23: 199-206., Muñoz et al. 2012Muñoz I., García-Isarch E., Sobrino I., et al. 2012. Distribution, abundance and assemblages of decapod crustaceans in waters off Guinea-Bissau (north-west Africa). J. Mar. Biolog. Assoc. U.K. 92: 475-494. https://doi.org/10.1017/S0025315411001895 , Castillo et al. 2014Castillo S., de Matos Pita S.S., Ramil F. 2014. Decapods assemblages in deep Mauritanian waters. Simposio Internacional de Ciéncias del Mar.). A similar segregation has also been detected for cephalopods (Quetglas et al. 2000Quetglas A., Carbonella A., Sánchez P. 2000. Demersal Continental Shelf and Upper Slope Cephalopod Assemblages from the Balearic Sea (North-Western Mediterranean). Biological Aspects of Some Deep-Sea Species. Estuar. Coast. Shelf Sci. 50: 739-749. https://doi.org/10.1006/ecss.1999.0603 , González and Sánchez 2002González M., Sánchez P. 2002. Cephalopod assemblages caught by trawling along the Iberian Peninsula Mediterranean coast. Sci. Mar. 66: 199-208. https://doi.org/10.3989/scimar.2002.66s2199 , Ciércoles et al. 2018Ciércoles C., García-Ruiz C., González M., et al. 2018. Molluscs collected with otter trawl in the northern Alboran Sea: main assemblages, spatial distribution and environmental linkage. Mediterr. Mar. Sci. 19: 209-222. https://doi.org/10.12681/mms.2124 ), fish (Gouraguine et al. 2011Gouraguine A., Hidalgo M., Moranta J., et al. 2011. Elasmobranch spatial segregation in the western Mediterranean. Sci. Mar. 75: 653-664. https://doi.org/10.3989/scimar.2011.75n4653 , García-Ruiz et al. 2015García-Ruiz C., Lloris D., Rueda J.L., et al. 2015. Spatial distribution of ichthyofauna in the northern Alboran Sea (western Mediterranean). J. Nat. Hist. 49: 1191-1224. https://doi.org/10.1080/00222933.2014.1001457 , Ramírez-Amaro et al. 2015Ramírez-Amaro S., Ordines F., Terrasa B., et al. 2015. Demersal chondrichthyans in the western Mediterranean: assemblages and biological parameters of their main species. Mar. Freshw. Res. 67: 636-652. https://doi.org/10.1071/MF15093 ) and megabenthic fauna (Abad et al. 2007Abad E., Preciado I., Serrano A., Baro J. 2007. Demersal and epibenthic assemblages of trawlable grounds in the northern Alboran Sea (western Mediterranean). Sci. Mar. 71: 513-524. https://doi.org/10.3989/scimar.2007.71n3513 ), highlighting the importance of depth as a structuring factor in marine communities of the Mediterranean Sea.

The continental shelf assemblages (IS and OS) showed a high level of overlap between each other because they shared the most dominant species, but the two slope assemblages (US and MS) displayed marked differences and different dominant species. These greater differences in the slope assemblages could be attributed to some hydrological differences between the two depth strata (Abelló et al. 1988Abelló P., Valladares F.J., Castellón A. 1988. Analysis of the structure of decapod crustacean assemblages off the Catalan coast (North-West Mediterranean). Mar. Biol. 98: 39-49. https://doi.org/10.1007/BF00392657 ). Although a thermally stable environment can be assumed below 200 m in the Mediterranean Sea (Hopkins 1985Hopkins T.S. 1985. Physics of the sea. In: Margalef R. (ed), Key environments: Western Mediterranean. Pergamon Press, pp. 100-125.), small changes in some environmental parameters (such as salinity) must be present at the species level, affecting their distribution and abundance, as shown in other studies (García-Rodríguez et al. 2011García Rodríguez M., Abelló P., Fernández A., Esteban A. 2011. Demersal Assemblages on the Soft Bottoms off the Catalan-Levante Coast of the Spanish Mediterranean. J. Mar. Biol. 2011: 1-16. https://doi.org/10.1155/2011/976396 , Keller et al. 2017Keller S., Hidalgo M., Álvarez-Berastegui D., et al. 2017. Demersal cephalopod communities in the Mediterranean: a large-scale analysis. Mar. Ecol. Prog. Ser. 584: 105-118. https://doi.org/10.3354/meps12342 , Quattrocchi et al. 2020Quattrocchi F., Fiorentino F., Valentina L., Garofalo G. 2020. The increasing temperature as driving force for spatial distribution patterns of Parapenaeus longirostris (Lucas 1846) in the Strait of Sicily (Central Mediterranean Sea). J. Sea Res. 158: 101871. https://doi.org/10.1016/j.seares.2020.101871 ). Additionally, the dominant decapod species in each detected assemblage were similar to those found in the same area with the same sampling gear (Abelló et al. 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 ). This similarity could be related to the stability of the demersal structures over time, as shown by other authors in the Mediterranean Sea (Gaertner et al. 2005Gaertner J.C., Bertrand J.A, Gil de Sola L., et al. 2005. Large spatial scale variation of demersal fish assemblage structure on the continental shelf of the NW Mediterranean Sea. Mar. Ecol. Prog. Ser. 297: 245-257. https://doi.org/10.3354/meps297245 ).

The decapod assemblages displayed geographical differences in composition and structure between the sectors of the study area. Although sampling effort was different between sectors, the annual repeat of the same sampling stations and the long temporal database reinforce the idea that the differences between these sectors are mainly driven by differences in the composition and structure of decapod assemblages between sectors. The main differences were due to the pandalid shrimp P. heterocarpus, which was dominant in the OS assemblage of the northern Alboran Sea and Gulf of Vera sectors, but not at Alboran Island. Also, P. heterocarpus was far less abundant in the Alboran Island sector, and seemed to have a deeper and more restricted bathymetric range (328 to 566 m depth). This may be related to the influence of the nutrient-rich coastal upwellings present along the northern Alboran Sea sector, which allow the species to reach shallower waters (Carbonell et al. 2003Carbonell A., Palmer M., Abelló P., et al. 2003. Mesoscale geographical patterns in the distribution of pandalid shrimps Plesionika spp. in the Western Mediterranean. Mar. Ecol. Prog. Ser. 247: 151-158. https://doi.org/10.3354/meps247151 ). In contrast, P. edwardsii was more abundant in the US assemblage of the Gulf of Vera than in the same assemblage of other sectors, in agreement with García-Rodríguez et al. (2000)García Rodríguez M., Esteban A., Pérez Gil J. L. 2000. Considerations on the biology of Plesionika edwardsi (Brandt, 1851) (Decapoda, Caridea, Pandalidae) from experimental trap catches in the Spanish western Mediterranean. Sea. Sci. Mar. 64: 369-379. https://doi.org/10.3989/scimar.2000.64n4369 . Finally, a higher abundance of A. antennatus was detected in the MS assemblages of the Alboran Island and Gulf of Vera, probably because of the greater presence of submarine canyons in both sectors, which are a preferred habitat for this species (Martínez-Baños 1997Martínez-Baños P. 1997. Dinámica de poblaciones de la gamba Aristeus antennatus (Crustacea, Decapoda) en las zonas de Murcia, Almería e Ibiza. Análisis global en el Mediterráneo Español. PhD thesis, Univ. Murcia, 291 pp.). In fact, the presence of populations of A. antennatus attracts a large deep-water trawling fishery to Alboran Island, the northeastern part of the Alboran Sea and the Gulf of Vera (Sardà et al. 2004Sardà F., Calafat A., Flexas M. M., et al. 2004. An introduction to Mediterranean deep-sea biology. Sci. Mar. 68: 7-38 https://doi.org/10.3989/scimar.2004.68s37 ; García-Rodríguez 2003García Rodríguez M. 2003. La gamba roja Aristeus antennatus (Risso, 1816) (Crustacea, Decapoda): distribución, demografía, crecimiento, reproducción y explotación en el Golfo de Alicante, Canal de Ibiza y Golfo de Vera. Ph.D. thesis, Univ. Complutense de Madrid, 298 pp., Fernandez-Arcaya et al. 2019Fernandez-Arcaya U., Bitetto I., Esteban A., et al. 2019. Large-scale distribution of a deep-sea megafauna community along Mediterranean trawlable grounds. Sci. Mar. 83S1: 175-187. https://doi.org/10.3989/scimar.04852.14A ).

Although no sampling could be carried out in the present study at depths shallower than 100 m around Alboran Island (owing to the presence of a marine reserve), when we compared the fauna from shallow depths around the island (<100 m depth) with those in other geographical sectors found in other studies based on beam-trawl samples (Gofas et al. 2014Gofas S., Goutayer J., Luque Á.A., et al. 2014. Espacio Marino de Alborán. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, 129 pp.), we observed that the hermit crab D. arrosor is the only dominant species shared by all three sectors. The rest of the dominants decapods in the shallow sedimentary habitats around the island, such as Scyllarus pygmaeus, the hermit crab Paguristes eremita and several species of crabs of the genus Pisa, were absent or displayed low abundances on the continental shelf of the northern Alboran Sea. These differences in the dominant species are probably due to the fact that the sedimentary habitats in the island are mainly composed of bioclastic and coarse sands and rhodoliths, which are less common on the continental shelf, where muddier bottoms generally occur (Gofas et al. 2014Gofas S., Goutayer J., Luque Á.A., et al. 2014. Espacio Marino de Alborán. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, 129 pp.).

In the present study, the composition of the decapod assemblages of the shallowest strata (shelf) of the Alboran Sea is similar to those of other parts of the Mediterranean Sea and adjacent Atlantic waters. Similar dominant species (but with a different percentage of contribution) were found for the shelf (IS, OS) and US assemblages of the Alboran Sean in comparison with other Mediterranean areas (Abelló et al. 1988Abelló P., Valladares F.J., Castellón A. 1988. Analysis of the structure of decapod crustacean assemblages off the Catalan coast (North-West Mediterranean). Mar. Biol. 98: 39-49. https://doi.org/10.1007/BF00392657 , 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 , García-Rodríguez et al. 2011García Rodríguez M., Abelló P., Fernández A., Esteban A. 2011. Demersal Assemblages on the Soft Bottoms off the Catalan-Levante Coast of the Spanish Mediterranean. J. Mar. Biol. 2011: 1-16. https://doi.org/10.1155/2011/976396 , Deval et al. 2017Deval M., Yilmaz S., Kapiris K. 2017. Spatio Temporal Variations in Decapod Crustacean Assemblages of Bathyal Ground in the Antalya Bay (Eastern Mediterranean). Turkish J. Fish. Aquat. Sci. 17: 967-979. https://doi.org/10.4194/1303-2712-v17_5_12 ). One exception was detected in those of the Italian margin of the Tyrrhenian sea, where D. arrosor was scarce or not recorded at all (Fanelli et al. 2007Fanelli E., Colloca F., Ardizzone G. 2007. Decapod crustacean assemblages off the West coast of central Italy (western Mediterranean). Sci. Mar. 71: 19-28. https://doi.org/10.3989/scimar.2007.71n119 ). Moreover, it is worth mentioning that P. longirostris showed a different bathymetric range between the Alboran Sea and the Tyrrhenian Sea, being more abundant in shallower waters characterizing the OS assemblages (<200 m) in the latter (Fanelli et al. 2007Fanelli E., Colloca F., Ardizzone G. 2007. Decapod crustacean assemblages off the West coast of central Italy (western Mediterranean). Sci. Mar. 71: 19-28. https://doi.org/10.3989/scimar.2007.71n119 ). Some authors have suggested that the main drivers of high abundances of P. longirostris are the increase in water temperature (Quattrocchi et al. 2020Quattrocchi F., Fiorentino F., Valentina L., Garofalo G. 2020. The increasing temperature as driving force for spatial distribution patterns of Parapenaeus longirostris (Lucas 1846) in the Strait of Sicily (Central Mediterranean Sea). J. Sea Res. 158: 101871. https://doi.org/10.1016/j.seares.2020.101871 ), the interaction between wind and current circulations (Ligas et al. 2011Ligas A., Sartor P., Colloca F. 2011. Trends in population dynamics and fishery of Parapenaeus longirostris and Nephrops norvegicus in the Tyrrhenian Sea (NW Mediterranean): the relative importance of fishery and environmental variables. Mar. Ecol. 32: 25-35. https://doi.org/10.1111/j.1439-0485.2011.00440.x ), high salinity (Benchoucha et al. 2008Benchoucha S., Berraho A., Bazari H., Katara I., et al. 2008. Salinity and temperature as factors controlling the spawning and catch of Parapenaeus longirostris along the Moroccan Atlantic Ocean. Hydrobiologia 612: 109-123. https://doi.org/10.1007/s10750-008-9485-y ) and high primary productivity (Colloca et al. 2004Colloca F., Carpentieri P., Balestri E., Ardizzone G.D. 2004. A critical habitat for Mediterranean fish resources: shelf-break areas with Leptometra phalangium (Echinodermata: Crinoidea). Mar, Biol. 145: 1129-1142. https://doi.org/10.1007/s00227-004-1405-8 ). Regarding the deepest assemblages, differences were detected between those of the northern Alboran Sea and others parts of the Mediterranean and adjacent Atlantic water. The dominant species in the deepest assemblage (MS) of the present study were mostly different from those of the central and eastern Mediterranean Sea, where A. antennatus, N. norvegicus, Aristaeomorpha foliacea and P. martia are dominant (Fanelli et al. 2007Fanelli E., Colloca F., Ardizzone G. 2007. Decapod crustacean assemblages off the West coast of central Italy (western Mediterranean). Sci. Mar. 71: 19-28. https://doi.org/10.3989/scimar.2007.71n119 , Deval et al. 2017Deval M., Yilmaz S., Kapiris K. 2017. Spatio Temporal Variations in Decapod Crustacean Assemblages of Bathyal Ground in the Antalya Bay (Eastern Mediterranean). Turkish J. Fish. Aquat. Sci. 17: 967-979. https://doi.org/10.4194/1303-2712-v17_5_12 , Fernandez-Arcaya et al. 2019Fernandez-Arcaya U., Bitetto I., Esteban A., et al. 2019. Large-scale distribution of a deep-sea megafauna community along Mediterranean trawlable grounds. Sci. Mar. 83S1: 175-187. https://doi.org/10.3989/scimar.04852.14A ). This fact contributes to the faunistic differentiation of the Alboran Sea, which is important for fisheries management. The rare presence of A. foliacea in the Alboran Sea, with only one individual captured in the present study, is noteworthy and similar to the observations made in the southern Alboran Sea, where just one record was observed some decades ago (Maurin 1962Maurin C. 1962. Etude des fonds chalutables de la Mediterranee occidentale (ecologie et peche) «Président-Théodore-Tissier» 1957 à 1960 et «Thalassa» 1960 et 1961. Rev. Trav.’Inst. Pêches Mari. (0035-2276) (ISTPM), 1962-06 26: 163-218.). The small populations of A. foliacea in the study area could be related to environmental drivers because its abundance declines with temperature and salinity rises, as detected in the western Mediterranean basin (Balearic Basin) (Cartes et al. 2011Cartes J. E., Maynou F., Abelló P., et al. 2011. Long-term changes in the abundance and deepening of the deep-sea shrimp Aristaeomorpha foliacea in the Balearic Basin: relationships with hydrographic changes at the Levantine Intermediate Water. J. Mar. Syst. 88: 516-525. https://doi.org/10.1016/j.jmarsys.2011.07.001 , 2014Cartes J. E., Fanelli E., Kapiris K., et al. 2014. Spatial variability in the trophic ecology and biology of the deep-sea shrimp Aristaeomorpha foliacea in the Mediterranean Sea. Deep-Sea Res. Part I: Oceanogr. Res. Pap. 87: 1-13. https://doi.org/10.1016/j.dsr.2014.01.006 ). The continental slope decapod assemblages of the northern Alboran Sea are also well differentiated from those in adjacent areas of the Atlantic Ocean. Only one decapod, S. membranacea, was shared with the slope assemblages of southern Spain (Gulf of Cádiz), which are dominated by N. norvegicus, Philocheras echinulatus, S. membranacea, Processa canaliculata and P. sivado (López de la Rosa 1997López de la Rosa I. 1997. Crustáceos decápodos capturados durante las campañas del IEO ARSA 0393 y ARSA 1093 en el golfo de Cádiz: distribución batimétrica. Publ. Espec. Inst. Esp. Oceanogr. 23: 199-206.). In the Atlantic waters of northwest Africa, the slope assemblages (200-500 m depth) displayed a lower contribution of P. longirostris and P. heterocarpus than those found in the present study (Muñoz et al. 2012Muñoz I., García-Isarch E., Sobrino I., et al. 2012. Distribution, abundance and assemblages of decapod crustaceans in waters off Guinea-Bissau (north-west Africa). J. Mar. Biolog. Assoc. U.K. 92: 475-494. https://doi.org/10.1017/S0025315411001895 ). Moreover, two dominant species, P. narval and D. arrosor, were shown to share the US assemblages and another two (P. martia and Polycheles typhlops) share the MS assemblage in the Canary Islands (González-Pajuelo et al. 2006González-Pajuelo J., González J.A., Lorenzo J.M., et al. 2006. Assemblages of the bathyal decapod crustaceans community in the Canary Islands. XIV Simposio Ibérico de Estudios de Biología Marina (SIEBM). Barcelona, 2 pp.).

Regarding ecological indices, GAM analyses showed clear depth trends for the four ecological indices: abundance, species richness, Shannon-Wiener diversity and Pielou’s evenness. Decapod abundance increased with depth, peaking around 200 m, which is related to the high abundance of some gregarious dominant species, such as P. heterocarpus. Species richness also increased with depth, peaking at 400 to 500 m, thus making the US assemblage a transition zone with the coexistence of characteristic species from adjacent shallow and deep assemblages, in agreement with the findings for other faunal groups in the northern Alboran Sea, such as molluscs (Ciércoles et al. 2018Ciércoles C., García-Ruiz C., González M., et al. 2018. Molluscs collected with otter trawl in the northern Alboran Sea: main assemblages, spatial distribution and environmental linkage. Mediterr. Mar. Sci. 19: 209-222. https://doi.org/10.12681/mms.2124 ). However, Shannon-Wiener diversity and Pielou’s evenness decreased with depth, with a minimum at 200 m, but increased afterwards. These results could be related to the fact that the OS assemblage was characterized by few, very abundant species, while the slope assemblages showed a higher number of species which were less dominant. Similar results were found by Mateo-Ramírez et al. (2015)Mateo-Ramírez Á., Farias C., Gallardo Roldán H., et al. 2015. Asociaciones de decápodos de fondos blandos circalitorales y batiales del mar de Alborán. In: Díaz del Rio V., Bárcenas P., et al. (eds), Volumen de Comunicaciones presentadas en el VII Simposio sobre el Margen Ibérico Atlántico. Sia Graf, Málaga, pp. 433-436. in the northern Alboran Sea, by Cartes and Sardà (1992)Cartes J.E., Sardà F. 1992. Abundance and diversity of decapods crustaceans in the deep-Catalan Sea (Western Mediterranean). J. Nat. Hist. 26: 1305-1323. https://doi.org/10.1080/00222939200770741 and Fanelli et al. (2007)Fanelli E., Colloca F., Ardizzone G. 2007. Decapod crustacean assemblages off the West coast of central Italy (western Mediterranean). Sci. Mar. 71: 19-28. https://doi.org/10.3989/scimar.2007.71n119 in the western and Central Mediterranean Sea, and by López de la Rosa (1997)López de la Rosa I. 1997. Crustáceos decápodos capturados durante las campañas del IEO ARSA 0393 y ARSA 1093 en el golfo de Cádiz: distribución batimétrica. Publ. Espec. Inst. Esp. Oceanogr. 23: 199-206. and Muñoz et al. (2012)Muñoz I., García-Isarch E., Sobrino I., et al. 2012. Distribution, abundance and assemblages of decapod crustaceans in waters off Guinea-Bissau (north-west Africa). J. Mar. Biolog. Assoc. U.K. 92: 475-494. https://doi.org/10.1017/S0025315411001895 in Atlantic waters. The increased environmental stability of the deep areas is likely to be a potential explanation for a high diversity (Sanders and Hessler 1969Sanders H. L., Hessler R. R. 1969. Ecology of the deep-sea benthos. Science 163:1419-1424. https://doi.org/10.1126/science.163.3874.1419 , Rex 1973Rex M.A. 1973. Deep-sea species diversity: decreased gasteropod diversity at abyssal depths. Science 181: 1051-1053. https://doi.org/10.1126/science.181.4104.1051 ), which may allow the development of a more mature and complex assemblage, as indicated by Abelló et al. (1988)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. 98: 39-49. https://doi.org/10.1007/BF00392657 .

The four GAM models also revealed geographical effects (a combination of longitude and latitude), with a greater abundance, species richness and Shannon diversity index in the westernmost part of the Alboran Sea, probably related to the high productivity associated with the major nutrient-rich coastal upwellings in this area (Rubín et al. 1997Rubín J. P., Cano N., Rodríguez V., et al. 1997. Relaciones del ictioplancton con la hidrología, biomasa fitoplanctónica, oxígeno disuelto y nutrientes, en el mar de Alborán y estrecho de Gibraltar (julio de 1993). Publ. Espec. Inst. Esp. Oceanogr. 24: 75-84., Sarhan et al. 2000Sarhan T., García-Lafuente J., Vargas J.M., Plaza F. 2000. Upwelling mechanisms in the northwestern Alboran Sea. J. Mar. Syst. 23: 317-331. https://doi.org/10.1016/S0924-7963(99)00068-8 ), the nutrient-rich water transport through the strait of Gibraltar, and the cyclonic vorticity that accumulates nutrients and produces permanent fertilization in the westernmost part of the Alboran Sea (Skliris and Beckers 2009Skliris N., Beckers J.M. 2009: Modelling the Gibraltar Strait/Western Alboran Sea ecohydrodynamics. Ocean Dyn. 59: 489-508. https://doi.org/10.1007/s10236-009-0185-6 , Vargas-Yáñez et al. 2019Vargas-Yáñez M., García-Martínez M.C., Moya, F., et al. 2019. The present state of marine ecosystems in the Spanish Mediterranean in a climate change context. Grupo Mediterráneo de Cambio Climático. 185 pp.). Similarly, a high diversity was detected in the easternmost part, which is a transition area with the coexistence of Mediterranean and Atlantic species. Slight temporal patterns were found for abundance and species richness. However, the present study showed the absence of consistent temporal trends and the presence of annual oscillations of the decapod assemblages in the study area. Temporary changes in the abundance of benthic and demersal species could be the result of biological processes, such as recruitment, mortality and predation, in addition to variations in the fishing impact (increased or decreased fishing effort) in some commercial decapod species or even in commercial species feeding on decapods (Snelgrove and Butman 1994Snelgrove P.V., Butman C.A. 1994. Animal-sediment relationships revisited: Causes versus effect. Oceanogr.Mar. Biol. 32: 111-177., Ólafsson et al. 1994Ólafsson E. B., Peterson C. H., Ambrose Jr W. G. 1994. Does recruitment limitation structure populations and communities of macro-invertebrates in marine soft sediments: the relative significance of pre-and post-settlement processes. Oceanogr. Mar. Biol. Ann. Rev. 32:65-109.).

The results of the present study improve knowledge of the decapod assemblages inhabiting the trawlable bottoms of a specific part of the European margin and the western Mediterranean Sea. The study area corresponds to the geographical subareas GSA01 and GSA02 established by the General Fisheries Commission for the Mediterranean (GFCM) for fishing management. Faunistic studies are an essential tool in managing fisheries, especially because both fisheries management and conservation policies apply to an ecosystem-based approach (Pikitch et al. 2004Pikitch E.K., Santora C., Babcock E.A., et al. 2004. Ecosystem-Based Fishery Management. Science 305: 346-347. https://doi.org/10.1126/science.1098222 , Bellido et al. 2011Bellido J.M., Santos M.B., Grazia M., Valeiras X., Pierce J.G. 2011. Fishery discards and bycatch: solutions for an ecosystem approach to fisheries management? Hydrobiologia 670: 317-333. https://doi.org/10.1007/s10750-011-0721-5 ). Moreover, this study provides a baseline for characterizing specific components (decapod crustaceans in this case) of benthic and demersal communities on sedimentary habitats under the framework of the Marine Strategy Framework Directive (MSFD, 2008/56/EC). This is especially important in areas with a high marine diversity that are regarded as self-standing ecoregions, such as the Alboran Sea (Abelló et al. 2002Abelló P., Carbonell A., Torres P. 2002. Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Sci. Mar. 66 (Suppl. 2): 183-198. https://doi.org/10.3989/scimar.2002.66s2183 , Spalding et al. 2007Spalding M., Fox H., Allen G., et al. 2007. Marine Ecoregions of the World: A Bioregionalization of Coastal and Shelf Areas. BioScience. 57: 573-583. https://doi.org/10.1641/B570707 , Coll et al. 2010Coll M., Piroddi C., Steenbeek J., et al. 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns and Threats. PloS ONE 5:e11842. https://doi.org/10.1371/journal.pone.0011842 ).