Ampelisca lusitanica (Crustacea: Amphipoda): new species for the Atlantic coast of Morocco

This study reports for the first time the presence of the Lusitanian ampeliscid amphipod Ampelisca lusitanica Bellan-Santini & Marques, 1986 in the northwestern Atlantic coast of Morocco. Specimens were collected in January 2015 from intertidal rock pools along the El Jadida shoreline associated with the brown algae Bifurcaria bifurcata and Sargassum muticum. Systematic description of the species is presented, as well as a discussion of its ecological and geographical distribution. This new finding extends the geographical distribution from the Lusitanian (Europe) to the Mauritanian (Africa) region and increases knowledge of the ecology and the global distribution of A. lusitanica found, previously, only on Portuguese and Spanish coasts.


Introduction
Crustacean amphipods are distributed in all ecosystems worldwide including terrestrial, freshwater and marine aquatic environments (Mosbahi et al. 2015). They often play a critical role in aquatic food webs, acting as conduits of nutrients and energy to higher trophic levels (Vainola et al. 2008). The Ampeliscidae is one of the most diversified amphipod families in the ocean (Barnard and Karaman 1991). This family is commonly found in a variety of habitats from shallow to deep waters although some species are restricted to limited bathymetric ranges and sediment types (Dauvin et al. 2012). Ampeliscid communities are generally composed of several species belonging to three dominant genera: Ampelisca, Byblis, and Haploops. The genus Ampelisca Krøyer, 1842 is a diverse benthic genus of marine amphipods, containing approximately 236 species (WORMS 2017) mainly reported from shallow waters with a worldwide distribution (Dauvin 1988;Dauvin and Bellan-Santini 1988;Filhoa et al. 2009;Dauvin et al. 2012). In the northeastern Atlantic region between the northern coast of Norway and the Gulf of Guinea, Ampelisca is represented by more than 52 valid species (Dauvin and Bellan-Santini 1988). Ampelisca species are found from the intertidal zone to abyssal depths, but most of them live on the continental shelf (Bellan-Santini and Dauvin 1988a;Dauvin 1988;Dauvin and Bellan-Santini 1988). Among Ampelisca species, the Lusitanian marine amphipod Ampelisca lusitanica Bellan-Santini and Marques, 1986 was reported first from the Atlantic coast of Portugal (Bellan-Santini and Marques 1986) and later from the northeastern Atlantic coast of Spain (Martínez et al. 2007).
The present paper reports the first discovery of A. lusitanica in North African Atlantic marine waters (littoral of El Jadida, NW Morocco). Some data on the external morphology, ecology and distribution of the species are provided.

Material and methods
Samples were collected as a part of a study on macroalgae-associated epifauna in the northwestern Atlantic coast of Morocco. Seaweed species were carefully removed from the intertidal substratum, and placed in plastic bags with 5% formalin. In the laboratory, macroalgae were washed in fresh water to collect the majority of the associated fauna. Specimens were sieved (0.5 mm mesh size), sorted and preserved (70% ethanol) for later identification and counting. Ampelisca lusitanica specimens were conserved separately, examined and identified according to descriptions provided by Bellan-Santini and Marques (1986), and Dauvin and Bellan-Santini (1988).

Description
A. lusitanica can be distinguished from other Ampelisca species by the following characters ( Fig. 2): The head is obliquely truncated, shorter than the three first segments of the pereon. The lower pair of eyes set at lower front corners of the head. The first antenna is shorter than A2 reaching the middle of its flagellum. The latter is about half the length of the body (Fig. 2a, b). The third epimeral plate is rounded-quadrate at the postero-distal corner. Pereopod 7 has the basis distally rounded; the merus (without a large posterior lobe) is shorter than the carpus with an anterior peg-like process projecting beyond the proximal end of the carpus but not reaching its distal end; the dactylus is rounded and slightly curved in its terminal part (Fig. 2c). The first and second uropods have spinous inner and outer rami. The inner ramus of the uropod 3 is longer than the outer ramus, with its inner margin denticulate (10-12 denticulations). A. lusitanica can be confused with A. unidentata Schellenberg, 1936 (Bellan-Santini and Marques 1986) but the latter differs from the former by antenna formula (Al sub-equal to A2) and the epimeral plate 3 which has postero-distal corner quadrate.

Discussion
The amphipod A. lusitanica was considered as an uncommon to rare species for Portuguese coasts and the Lusitanian region (Bellan-Santini and Dauvin 1988a,b;Marques and Bellan-Santini 1990), and southeast of the Bay of Biscay, Spain (Martínez et al. 2007). This species is known as typical of coastal warm temperate waters and occurs in various habitats. It was found on deep rocky bottoms (between 8 and 37 m) (Bellan-Santini and Marques 1986; Bellan-Santini and Dauvin 1988a,b) covered with sand or silt and on intertidal rocky substrates with algal communities such as Corallina elongata, Jania rubens and Cystoseira sp. (Bellan-Santini and Marques 1986). The species was also reported from muddy bottoms at 7.5 km upstream from the mouth river of the Mira estuary where the salinity is lower than in open coastal waters (Marques and Bellan-Santini 1987) and from sandy sediments of continental shelf of Guipúzcoa at 41 m depth from Basque Country, Spain (Martínez et al. 2007). However, in the present investigation, A. lusitanica was found associated to the brown seaweeds Bifurcaria bifurcata and Sargassum muticum on protected rocky intertidal pools of 1-4 m depth where surface seawater temperature ranged between 16 and 20°C and salinity varied from 33 to 37‰. According to Bellan-Santini and Marques (1986), the ecology of A. lusitanica seems to be similar to that of A. rubra Chevreux, 1925 (accepted name Ampelisca heterodactyla Schellenberg, 1925), A. serraticaudata Chevreux, 1888 and especially A. unidentata Schellenberg, 1936. Based on the literature data, the geographical distribution of this species (Fig. 1) would seem to be currently limited to the North-east Atlantic region particularly to the Portuguese coast (Marques and Bellan-Santini 1987;Bellan-Santini and Dauvin 1988a;Marques and Bellan-Santini 1990;Bellan-Santini and Costello 2001) and the Basque Country, Spain (Martínez et al. 2007). Like most Ampelisca species, A. lusitanica is restricted to small geographical areas. It had previously only been reported thrice inside the Lusitanian region; twice from coastal waters of Portugal (Bellan-Santini and Marques 1986;Marques and Bellan-Santini 1987) and once from southeast of the Bay of Biscay, Spain (Martínez et al. 2007). The species was not found in the Azores archipelago (Portugal), located in the middle north Atlantic region (Rosa Lopes et al. 1993) nor in the eastern side of the Iberian Peninsula, western Mediterranean (Conradi and López-González 1999;de-la-Ossa-Carretero et al. 2010, 2016. Also the species was not reported from the Portuguese continental shelf during a comprehensive sampling of the soft-bottom macrofauna (Martins et al. 2013). This is the first record of the species outside its native geographical area (Lusitanian region) and the third one at the regional scale (NE Atlantic).
Due to the presence of A. lusitanica in a wide range of habitats and its ability to support varying environmental conditions in intertidal and in subtidal deeper areas, we assume that the species could occur in other coastal localities away from its previously recorded biogeographic region (Lusitanian). Wherever encountered it is always a rare species with low abundances.
The lack of previous records in Morocco and North Africa might be due to the small size of individuals, the low abundance of local populations, or its misidentification (including a possible confusion with its congeneric species Ampelisca unidentata). Also, the limited distribution of the species might be due to an insufficient investigation effort.
Significant numbers of individuals of A. lusitanica were found with B. bifurcata (5 individuals), whereas only one individual was found on S. muticum. It can be suggested that the complexity of the algal habitat was not an important factor affecting the abundance of A. lusitanica. Previous studies showed that the structural complexity of algae was not a consistent predictor of the number of individuals and species of amphipods (Russo 1990;Schreider et al. 2003;Engelen et al. 2013). Conversely, Taylor and Cole (1994) and Wernberg et al. (2004) reported a higher abundance of small crustaceans in more structurally complex algal habitats. The number of individuals found associated with intertidal algal samples in the present investigation corroborates results obtained by Bellan-Santini and Marques (1986) on the Portuguese coast, where the lower number of specimens ranging from 2 to 5 individuals, was reported from intertidal habitats and the higher number (up to 28 individuals) was recorded from the deeper areas (37 m depth) where a more stable environment accounted for higher species abundances.
This study reported on the first record of A. lusitanica in Moroccan waters (i) suggests that A. lusitanica may also be present in other localities of Moroccan shores, (ii) extends the geographical range of the species A. lusitanica into the northeastern Atlantic (species shifting from the Lusitanian region), (iii) adds a new contribution to the macrofauna diversity thriving in seaweed beds and (iv) yields a contribution to the growing body of knowledge of the Moroccan and North African Atlantic biodiversity.