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Caridea: Hippolytidae

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Caridea: Hippolytidae Manuscript Click here to view linked References 1 TITLE: Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis 2 and Maurin, 1952 (Caridea: Hippolytidae), a potential amphi-Atlantic species: 3 implications of global climate change in marine fauna conservation 4 5 Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and 6 Maurin, 1952 (Caridea: Lysmatidae). 7 8 RUNNING TITLE: Lysmata uncicornis across Atlantic waters 9 10 E. GONZÁLEZ-ORTEGÓN1*, J. E. GARCÍA-RASO2, R. CALADO3, I. LÓPEZ DE 11 LA ROSA1, M. GUERRERO4 and J.A. CUESTA1 12 13 1Instituto de Ciencias Marinas de Andalucía, CSIC, Avda. República Saharaui, 2, 11519 14 Puerto Real, Cádiz, Spain 15 2Universidad de Málaga, Departamento de Biología Animal, Facultad de Ciencias, 16 Campus de Teatinos s/n, Málaga, Spain 17 3ECOMARE, Centre for Environmental and Marine Studies (CESAM), Department of 18 Biology, University of Aveiro, Santiago University Campus, 3810-193 Aveiro, Portugal 19 4Facultad de Ciencias del Mar y Ambientales, Universidad de Cádiz, Puerto Real, 20 Cádiz, Spain 21 *Corresponding Author: Enrique González-Ortegón 22 [email protected] 23 24 Tel.: +34 956832612; fax: +34 956 83 47 01 25 26 May 2019 27 Abstract 28 29 The present study reports the occurrence of several specimens of the African caridean 30 shrimp Lysmata uncicornis Holthuis and Maurin, 1952 in the NE Atlantic coast (Gulf of 31 Cadiz, Spain and the Algarve, Portugal). Lysmata uncicornis is a poorly studied species 32 that has been originally described from the Atlantic waters of Morocco, where it was 33 first collected inside the port of Casablanca in a rocky bottom at 4-5 m depth. While no 34 scientific publication has previously reported this species outside the waters of 35 Morocco, several specimens have been collected in the coastal waters of the Gulf of 36 Cadiz and the Algarve. This species may be able to expand successfully northward 37 along European waters, probably favoured by global warming. It is possible that this 38 expansion may also be enhanced through the marine aquarium trade. Recently, Lysmata 39 arvoredensis Giraldes, Macedo, Brandão, Baeza and Freire, 2018 a new species of 40 shrimp from the south coast of Brazil was described. However, morphological and 41 genetic comparisons revealed no differences between L. uncicornis and L. arvoredensis. 42 Therefore, L. arvoredensis should be considered as a junior synonym of L. uncicornis. 43 While L. uncicornis may well be an amphi-Atlantic species, such as L. grabhami 44 (Gordon 1935), for now, the introduction of L. uncicornis in Brazilian waters cannot be 45 ruled out. 46 47 Keywords: cleaner shrimp, Atlantic waters, Lysmata arvoredensis, amphi-Atlantic, 48 marine ornamental shrimp, introduced species, exotic species, tropicalization, 49 ornamental species, marine aquarium trade 50 51 1 52 Introduction 53 It is commonly reported that more non-native species occur rather at higher than lower 54 latitudes than that of their native home ranges (Guo et al. 2012). Several African species 55 are currently moving northward and arriving to Southwest European coasts, likely due 56 to global warming (e.g. Perez-Miguel et al. 2019). This natural expansion may 57 eventually be accelerated by other vectors, such as ballast water or human transactions. 58 As an example, one can refer the global trade of marine species for domestic and public 59 aquaria (Padilla and Williams 2004; Calado and Chapman 2006). Caridean shrimps 60 within genus Lysmata Risso, 1816 are commonly ranked among the top 10 most heavily 61 collected and traded marine ornamental invertebrates (Wabnitz et al. 2003). Coloration 62 is probably the most common feature used to recruit shrimp species to the marine 63 aquarium trade (see Calado et al. 2003 and Calado 2008 for details) and are likely one 64 of those invertebrate groups experiencing an increase in demand among hobbyists 65 (Calado et al. 2017). Despite the fact that biological invasions often contribute to native 66 biodiversity decline, and global warming and anthropogenic activities are expected to 67 elevate the potential of introducing non-native species worldwide, they continue to be 68 overlooked in marine conservation plans (Giakoumi et al., 2016). 69 70 Lysmata species, popularly termed as “peppermint shrimps”, occur worldwide in 71 tropical, warm to cold-temperate seas, usually on rocky boulder slopes and reef habitats, 72 being currently represented by 48 valid species (WoRMS, 2018), 24 of these being 73 present in the Atlantic Ocean (Western Atlantic: WA, Eastern Atlantic: EA) and 74 Mediterranean Sea (M). Chace (1997), Fransen (1991), d´Udekem d´Acoz (1999, 2000) 75 and Wirtz et al. (2016) have cited the following species to these geographic regions: 76 WA: L. anchisteus Chace, 1972, L. intermedia (Kingsley, 1878), L. rathbunae Chace, 77 1970 and L. wurdemanni (Gibbes, 1850); WA and EA: L. grabhami (Gordon, 1935) and 78 L. moorei (Rathbun, 1901); EA: L. olavoi Fransen, 1991, L. stenolepis Crosnier and 79 Forest, 1973 and L. uncicornis Holthuis and Maurin, 1952; EA and M: L. nilita Dohrn 80 and Holthuis, 1950 and L. seticaudata (Risso, 1816). Rhyne and Lin (2006) analysed 81 the complex L. wurdemanni and L. rathbunae for the WA and described 4 new species 82 for this region: L. ankeri Rhyne and Lin, 2006, L. bahia Rhyne and Lin, 2006, L. 83 pederseni Rhyne and Lin, 2006 and L. boggessi Rhyne and Lin, 2006, and redescribed 84 the species Lysmata rathbunae Chace, 1970 and L. wurdemanni. It is worth highlighting 85 that the presence of L. wurdemanni in WA is valid, but further studies are still needed 86 (Rhyne et al. 2009). More recently new Atlantic species have been described, namely L. 87 rafa Rhyne and Anker, 2007 from Florida (WA) (Rhyne and Anker 2007), L. hochi 88 Baeza and Anker 2008 from the Caribbean Sea (WA) (Baeza and Anker 2008), L. 89 jundalini Rhyne, Calado and Dos Santos, 2012 from Puerto Rico (WA) (Rhyne et al. 90 2012), L. udoi Baeza et al. 2009 from Venezuela (WA) (Baeza et al. 2009), L. baueri 91 Prakash and Baeza 2017 from Mexico (WA) (Prakash and Baeza 2017), Lysmata 92 napoleoni De Grave and Anker, 2018, from St. Helena (CA) (De Grave and Anker 93 2018) and Lysmata arvoredensis Girardes, Macedo, Brandão, Baeza and Freire, 2018 94 from Brazil (WA) (Giraldes et al. 2018). 95 In addition to the five species reported from the EA and the M, two alien 96 Lysmata species originating from the Indian Ocean have been reported for the M: L. 97 kempi Chace, 1997 (Froglia and Deval 2014) and L. vittata (Stimpson, 1860) 98 (Abdelsalam 2018). It is also worth highlighting that in the WA, namely in Brazil, the 2 99 alien species L. vittata has also been recorded and it was, at first, erroneously reported 100 as a new species: L. rauli Laubenheimer and Rhyne, 2010 (Soledade et al. 2013). 101 On what concerns the Atlantic waters of the Iberian Peninsula, only one species of 102 Lysmata has ever been officially documented: L. seticaudata (see Zariquiey Álvarez 103 1968; d’Udekem d’Acoz 1999). Another species that is also known to occur in this 104 region is L. nilita. This species has been recorded and collected in underwater caves at 105 Sagres in the Algarve (Ilhotes do Martinhal, 37º00'56"N 8º55'01"W) (southern 106 Portugal), but this finding has never been reported in the scientific literature (P. 107 Chevaldonné and R. Calado, personal observations). In the present study, we report the 108 occurrence of a third species of Lysmata in Atlantic Iberian waters: L. uncicornis. This 109 species that, was formerly solely known to occur in the Atlantic coasts of Morocco, has 110 expanded its range northward, from Morocco to the Gulf of Cadiz and the Algarve (SW, 111 Iberian Peninsula), likely as a consequence of ongoing ocean global warming with 112 potential implication on marine fauna conservation. 113 114 115 Material and Methods 116 Two specimens of L. uncicornis were collected in the coastal waters of Cadiz 117 (Spain) by traps for shrimp fishery at the breakwater pier close to the Naval Station 118 Rota (36°37'28.1"N 6°20'44.7"W) and one in Valdelagrana beach (36°33'24.5"N 119 6°13'45.8"W) in November 1997, five in the coastal waters of Portimão in the inner part 120 of the eastern breakwater pier at the entrance to Portimão harbour (37°06'33.30", N 121 8°31'26.50"W) in June 2017, and five at the breakwater pier at the entrance to Cadiz 122 harbour (36°32'33.05" N, 6°17'15.54"W) in January 2018 (Figure 1). 123 The specimens of L. uncicornis and L. seticaudata from Cadiz (Spain) and 124 Portimão (Portugal) examined in the present study were identified according to Holthuis 125 and Maurin (1952), Lagardère (1971), Chace (1997), Baeza and Anker (2008), Froglia 126 and Deval (2014), Anker and Cox (2011), Giraldes et al. (2018) and Abdelsalam (2018), 127 and photographed (Figure 3). Two specimens were deposited in the Decapoda and 128 Stomatopoda Crustacean Collection (Spanish Institute of Oceanography in Cadiz, 129 Spain) under catalogue numbers IEO-CD-CAD18/2463-2464 (see Table 1). 130 Two paratypes of L. uncicornis from Naturalis Biodiversity Centre, Leiden 131 (RMNH.CRUS.D.7812) collected in Casablanca, Morocco by Maurin in 1951, were 132 comparatively studied with Iberian L. uncicornis and sequenced (Table 1). 133 Total genomic DNA was extracted from pereiopod and/or pleon muscle tissue of 134 two specimens of Lysmata uncicornis and one of L. seticaudata, collected in Cadiz 135 harbour, and paratypes of L. uncirconis, following a modified Chelex 10% protocol by 136 Estoup et al.
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