Isopods (Crustacea, Malacostraca) from International Minho River, Iberian Peninsula

Nuno Miguel Araújo Gomes1,2*, Dimítri De Araújo Costa1,2, Harold Casalís Cantallo1, Tiago José Andrade Ribeiro1 and Carlos Antunes1,2 1Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Portugal 2Aquamuseu do Rio Minho, Parque do Castelinho, Portugal Submission: March 30, 2021; Published: May 07, 2021 Corresponding author: Nuno Miguel Araújo Gomes, Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, s/n, 4450-208 Matosinhos, Portugal. Email: Nuno@ciimar.up.pt


Introduction
Order Isopoda (Crustacea) is a diverse group with more than 10.000 valid species according to the World Register of Marine Species database [1], occupying all habitats from marine deep waters to freshwater aquifers or from deserts to mountains [2]. Isopods, known also as pillbugs, slaters and woodlice, represent a group of high range of polymorphism, characterized by a dorsoventrally compressed body shape, subdivided in three parts, a cephalon with two pairs of antennae, a pereon of seven segments with seven pairs of pereopods, a pleon of five segments with five pairs of pleopods, and a pleotelson with one pair of uropods [3]. Sexual dimorphism is present in some species, in which females carry the juveniles in a ventral marsupium; juveniles or manca lack the last pair of pereopods [2]. Meanwhile, deep sea individuals have adaptative structures, such as lack of eyes, antennae same or larger than body size, pereopods much larger than body size [4,5]. Some groundwater species with lateral compression [6], and loss of body shape in some parasitic species, i.e. pereonites become folded indistinct and with rudimentary or absent pereopods [7].
Portuguese isopod aquatic fauna remains poorly known despite recent taxonomic work, including groundwater species, e.g. [8][9][10], on shallow coastal waters e.g. and works from deep seas exploration expeditions on the continental Canyons and Portuguese archipelagos of Azores, e.g. [11][12][13]. Macroinvertebrate surveys on the Minho River started on 1982 [14], but have been scarce with only a few works on macrobenthic ecology or specimens collected through glass eel fishing bycatch [15][16][17]. In this study we provide diagnostics features for the isopod fauna collected on the Minho River estuary, belonging to 13 species, 10 genera, five families and three suborders, with ecological notes, global and Portuguese distributions, and a key for species identification.

Study Area
Minho River, located at the northwest of the Iberian Peninsula, originates in the Meira mountains (Spain), with around 300km of extension [18]. The international section located on the last 70km represents the northwest section Spanish/Portuguese border, culminating on an estuary flowing into the Northeast Atlantic Ocean. This estuary area has a length of approximately 40km, with a total area of 23km 2 [16], with a mesotidal partially mixed system tending towards a salt wedge estuary during the high floods [19], providing for a variety of habitats such as salt marshes, mudflats, sandflats and freshwater making for a high species diversity. Due

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Oceanography & Fisheries Open access Journal to its ecological importance, the international Minho River section (including the estuarine zone) was designated as a Natura 2000 site and as an Important Bird Area [20,21].
Isopod identification was based on specialized literature e.g. [3,7,23,24]. Synonym's compilation was performed, mainly according to WORMS database and data on species description compiled from taxonomic studies e.g. [25,26]. Type material and locality data were obtained from Global Biodiversity Information Facility [27] [29].

• Diagnosis
Anthurid with punctiform eyes; body elongated with keeled pereon; larger first pair of pereopods with a tooth on the inferior propodus margin; telson ovate gradually converging to a curved apex ( Figure 2B); antennules on both male and female of the same size; male with copulatory stylet on the second pleopod pair [3,26,27].

Global distribution
Northeast Atlantic Ocean; south and west coasts of England, South Wales, Ireland; southwest Baltic and Mediterranean [3].

Global Distribution
From the North Sea to Iberian Peninsula; British Isles and Mediterranean [3].

Ecological Notes
Found in sand beaches, on intertidal High Water Neap Tide (HWNT) zone to 60m depth; free movement with the rising tide and may be present among sand grains; feeding in the water column at high tide and at night [3].

• Remarks
Despite being typically found on sandy beaches, this marine species presence was probably due to drifting towards the net due to the flood tides entering the estuary.

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•

Type Material
Unknown. •

Global Distribution
Northeast Atlantic, from Scotland to Morocco [3]. •

Distribution in Portugal
Species recorded on Azores, Aveiro and the estuaries of the Mondego and Tejo rivers [35,46,43,47].

• Ecological Notes
Lives at estuarine muddy banks; late pranizas with parasitic behaviour on inshore or on flatfishes (order Pleuronectiformes); Adults occur in galleries, typically with a male near the entrance and 10 to 20 females on the inner part of the gallery [3,7].

• Diagnosis
Males pleotelson with two bosses joined at the bases, bidentate process sparsely rugose dorsally becoming narrower apically; females with pleotelson dome smoothly rounded on side view; length up to 7mm in males, 6mm in females [3,7,50]. •

Global Distribution
Northeast Atlantic from France and British Isles to Morocco, Tenerife, and Gran Canaria [50]. •

Distribution in Portugal
Species recorded along the West coast [33,57]. •

Ecological Notes
Common in rocky shores, from MTL to LWS; juveniles on intertidal algae that they feed upon; adults in rock crevices or empty tests of the barnacle Perforatus perforatus (Bruguière, 1789) in which they breed; each male usually with several females [3,50].

• Diagnosis
Pleotelson on males with two bosses fused by a stalk, in which each boss with a prominent, apical, subsidiary projection, bidentate processes apically tuberculate with similar width along their lengths ( Figure 3B); females with a mid-dorsal projection at posterior margin of pleotelson ( Figure 3C); maximum males' length 6mm, 4.8mm in females; lobes on maxillipedal palp thick, first longer than third [3,24]. •

Global Distribution
Northeast Atlantic, from France to the Iberian Peninsula; British islands; Macaronesian archipelagos; Mediterranean Sea along European and African coasts and Egypt [51]. •

• Diagnosis
First pleopod covers pleopods 2-5; pleon smooth and pleotelson with conspicuous tuberculation; pleotelson almost triangular shape, with the median region vaulted on both sides of the midline; apical foramen opens dorsally, visible as an open slit from above ( Figure 3E); both uropod rami apically rounded [54].

Distribution in Portugal
Species recorded along the West Portuguese coast [51]. •

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Found at marine shallow waters; usually associated with barnacles [54].

• Diagnosis
Pereopod 1 with around to 20 setae smooth-like on ischium and on merus; uropods with external margin of exopod almost smooth; pleotelson dorsal surface with two longitudinal rows of tubercles; antenna peduncle with 5 articles and flagellum with 12-16 articles ; interior endite of maxilliped with fringe of robust, plumose setae with swollen base on semi-circular distal margin; pleotelson subapically concave and slightly upcurved in side view; uropod reaching slightly beyond the posterior margin of pleotelson; maximum males length 10.5mm, 8.5mm in females [3,7,55].

Global Distribution
Northeast Atlantic from Poland, including Baltic Sea to Morocco; Mediterranean; Adriatic and Aegean Sea [54]. •

Distribution in Portugal
Species recorded on Aveiro [35] and on the Mondego estuary [46].

Ecological Notes
In estuaries near to upper limit of Extreme High-Water Springs (EHWS), euryhaline species, usually in ditches brackish water, on riverbanks, on muddy bottoms, under stones, and amongst seagrasses [3].

Global Distribution
Northeast Atlantic from Belgium to the Mediterranean and Southwest British coast [3,55].

• Ecological Notes
Brackish species occurring between Mean Tide Level (MTL) and Low Water Neap (LWN), under stones or in rock crevices [7].

Global Distribution
Northeast Atlantic from Sweden down to Morocco and Azores islands, also on Baltic Sea [54]. •

Ecological Notes
Brackish waters species common in sheltered estuarine situations, from MTL to EHWS occurring mostly on salt marshes with muddy substrates with aquatic vegetation, capable of surviving large fluctuations of temperature and salinity [3,7,55].

• Diagnosis
Palp segments 2-4 robust and lacking lobes, interior margins straight bearing dense fringes of long fine plumose setae; ischium of pereopod 1 with up to about 60 plumose setae in two rows, propodus with a distal row of 15-20 setae; pereopods 1-3 with

Global Distribution
Northeast Atlantic from British islands to Morocco; Mediterranean and Black Seas [55]. •

Ecological notes
Intertidal, often in sheltered places on High Water Springs (HWS) under stones or in crevices; around MTL on marine coasts [3,55].  •

Material Examined
PORTUGAL • 6 adults, size range 12 to 17mm, 5 juveniles, size range 4 to 6mm, coloration light brown with dark speckles or dark brown with lighter speckles; International Minho River,

Distribution in Portugal
Species recorded on the Minho River [16], Ria de Aveiro [34] and on the Mondego River [66].

Ecological Notes
Poorly known brackish waters species.

• Remarks
Species only known from the Northwest Iberian Peninsula except for the single specimen collected on the Guadalquivir estuary [64] requiring further investigation on distribution and ecology of this species.

• Diagnosis
Body slender adult males ranging 15mm, adult females from 6 to 10mm; antennule extending well beyond article 3 of antennal peduncle ( Figure 4E); antennal flagellum longer than the peduncle; narrow coxal plates, only those of pereonites 5-7 reaching the posterior border; pleotelson with sides subparallel, slightly curved in the mid-dorsal line; posterior border with a median tooth, hardly acute, and with obtuse lateral corners ( Figure 4F) [7]. •

Global Distribution
Northeast Atlantic from Norway down to Mediterranean [3]. •

Distribution in Portugal
Recorded in Ria de Aveiro [36], and on the Tejo River [35]. •

Ecological Notes
Brackish waters species common among intertidal waters in sheltered estuaries [7].

• Diagnosis
Pereon with triangular coxal plates and serrated lateral borders; pleotelson sides concave anteriorly, expanding about two-thirds of its length backwards, then narrowing sharply to an elongate median projection ( Figure 5D); males up to 22-25mm, female smaller [7].

Global Distribution
Northeast Atlantic coast from France to the Mediterranean and Southwest England [3]. •

Distribution in Portugal
Species recorded along the West coast [50,71] •

Ecological Notes
Usually found around algae and under stones on Low Water Slack Tide (LWST) [3].

Discussion
All species collected are within the boundaries of their known distribution, although most of them are new records for the Minho River estuary, mainly due to the lack of information on macroinvertebrates for this specific area. From the 248 specimens collected, 245 come from glass eel fishing bycatch, with an expected higher number of species and individuals for this method due to the area covered by the net, with specimens being sampled from the top of the water column to the bottom, and marine species drifting towards the net due to the flood tides entering the estuary [16].
Except for the species Cyathura carinata (Krøyer, 1847), Saduriella losadai Holthuis, 1964, Lekanesphaera levii (Leach, 1814) and Sphaeroma serratum (Fabricius, 1787) [15,16] all the other 9 species are new records for the international Minho River. The point of collection of S. serratum coincides with the samplings of this species [15,14]. Previous studies focused on ecological aspects, which contained lists of species, which in this manuscript some of these that were collected have been revised and morphologically described on taxonomic approach. Consequently, this is the first descriptive taxonomic study on Portuguese estuarine zone.
The most comparable study comes from Ria de Ferrol [72], on the Spanish Northwest coast approximately 200 km north from the Minho River estuary, where 39 isopod species were mentioned on a deep survey on the area studied. From the 13 species collected on the Minho River, 12 were also found on Ria de Ferrol only S. losadai being absent, with the northern most record on the Ulla River, Spain. A depth research is required to fully understand the composition and distribution of this group for the Portuguese coast, with different sampling methods concerning different habitats e assemblages.

Conclusion
This represents the first taxonomic study of Isopoda from the International Minho River, contributing for isopod Portuguese and Iberian fauna, due to localization of this river. Bycatch method was efficient for sampling these animals, which possibly indicates that other species could appear if the sampling effort were greater and regular over time. Minho River presents potentialities, still unknown, mainly in the descriptive aspect, that still need to be discovered, in view of its importance and its strategic position, flowing into the Atlantic Ocean.