Grandidierella Japonica (Amphipoda: Aoridae)

Munari et al. Marine Biodiversity Records (2016) 9:12 DOI 10.1186/s41200-016-0018-5 MARINE RECORD Open Access Grandidierella japonica (Amphipoda: Aoridae): a non-indigenous species in a Po delta lagoon of the northern Adriatic (Mediterranean Sea) Cristina Munari*, Nadia Bocchi and Michele Mistri Abstract Background: The introduction and spread of non-indigenous species is one of the main threats to biodiversity of aquatic ecosystems and it is becoming an increasing problem for the international scientific community. Aquaculture and related activities are recognized as one of the most important drivers of non-indigenous species in the Mediterranean. Grandidierella japonica Stephensen, 1938 is an aorid amphipod species native of Japan. This species had previously only been reported a few times outside the Pacific region, in particular from coastal waters of England and French Atlantic coasts. Results: A population of the non-indigenous amphipod G. japonica, has been detected in the Sacca di Goro, a Po delta lagoon of the northern Adriatic Sea (Italy), representing the first record of this species in the Mediterranean Sea. Adults of both sexes and juveniles were collected in muddy sediments reaching high densities. We examined 24 specimens: 8 adult males, 12 females, and 4 undifferentiated juveniles. Our specimens displayed a variability in the position of teeth of male gnathopod 1. Likely vectors for this introduction are the commercial shellfish transplants, mainly oyster farming. Conclusions: The finding of a reproducing population of G. japonica suggests that the species has become well established in the Sacca di Goro. This finding also seems to be particularly relevant for the improvement on the knowledge of Mediterranean biodiversity and threats. Keywords: Non-indigenous species, Amphipoda, Aoridae, Grandidierella japonica, Po delta lagoon, Mediterranean Sea Background Gollasch 2006), many of which are considered estab- Non-indigenous species introduction is one of the main lished (Zenetos et al. 2005). The reasons of the excep- threats to biodiversity of aquatic ecosystems; this is also tional susceptibility of the Mediterranean to biological an issue of growing concern in the marine and brackish invasions are: its long history of human occupation, contexts (Rosenthal 1980; Bax et al. 2003; Molnar et al. crisscrossing shipping lanes, many major ports and 2008). Aquaculture and related activities (e.g. sport innumerable marinas, lagoons and estuaries crowded fishing, fishery stock enhancement, ornamental trade) with fish and oyster farms, and shores that are major are recognized as important drivers of non-indigenous tourist destinations (Galil 2000). species in Europe (Olenin et al. 2008). Apart from the opening of the Suez Canal, the most The Mediterranean Sea, represents a hot spot of bio- prominent vector for species introduction to Europe and diversity, but it is also one of the major recipients of the Mediterranean Sea is shipping, combining ballast non-indigenous species (Galil 2000; Streftaris et al. 2005; water and hull fouling (Galil 2000; Gollasch 2006; Galil and Zenetos 2002). Aquaculture is the third most important means of introduction with unintentionally introduced * Correspondence: [email protected] Department of Life Science and Biotechnologies, University of Ferrara, Via species (e.g. fouling organisms on oyster) being more Borsari 46, 44121 Ferrara, Italy © 2016 Munari et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Munari et al. Marine Biodiversity Records (2016) 9:12 Page 2 of 8 numerous compared with those introduced intentionally This study reports of a dense population of the (Streftaris et al. 2005; Gollasch 2006). The north-western species G. japonica in the Sacca di Goro, a northern part of the Adriatic Sea is characterized by a large number Adriatic lagoon. This represents the first record of of brackish coastal lagoons, that are recognized as highly the species in the Mediterranean basin. This is also vulnerable to species introduction as a consequence of theonlymemberofthegenusGrandidierella their environmental instability, low number of species, ex- Coutière, 1904 to have been recorded, thus far, from ploitation for aquaculture and shellfish farming, and the the Mediterranean. Moreover, the finding of a repro- presence of not saturated benthic communities (Munari ducing population of this non-indigenous species and Mistri 2008). seems to be particularly relevant for the improvement Grandidierella japonica Stephensen, 1938 is an aorid on the knowledge of Mediterranean biodiversity and amphipod species (Crustacea: Amphipoda: Aoridae) native threats. We give some morphological details related of Japan (Chapman and Dorman 1975). Outside its native to the description of the species and some ecological area, this amphipod was reported at first only in the Pacific notes about this species and a discussion about its region: it occurred in San Francisco Bay (California) in possible vectors of introduction in the Mediterranean 1966 (Chapman and Dorman 1975), afterwards it was re- Sea. ported from intertidal and subtidal sediments of bays and estuaries of the western coast of North America from Results Mexico to Canada (Greenstein and Tiefenthaler 1997; Sampling stations were characterized by muddy (silty- Cohen et al. 1998; Cohen et al. 2002; Okolodkov et al. clay) sediments. Water (temperature, salinity and dis- 2007), and it has also been found in Hawaii (Coles et al. solved oxygen) and sediment (organic matter content 1999) and Australia (Myers 1981). Outside the Pacific re- and depth of the redox potential discontinuity layer) gion, reports of this species are from Southampton and the parameters at the 10 sampling stations are summa- Orwell Estuary, in south-eastern England (Smith et al. rized in Table 1. 1999; Ashelby 2006; Noël 2011). Recently it has been reported for the first time from the Atlantic coast of France, Systematics specifically from Marennes-Oléron Bay (Jourde et al. 2013) Order AMPHIPODA Latreille, 1816 and the Arcachon basin (Lavesque et al. 2014). G. japonica Suborder GAMMARIDEA Latreille, 1802 is not listed in the inventories for the Mediterranean Sea Family AORIDAE Stebbing, 1899 (Zenetos et al. 2005; Zenetos 2010; Zenetos et al. 2008; Genus Grandidierella Coutière, 1904 Zenetos et al. 2012; Galil 2008; Galil 2009), and EU data- Grandidierella japonica Stephensen, 1938 bases (DAISIE -Delivering Alien Invasive Species Inventor- (Figs. 1, 2 and 3) ies for Europe. http://www.europe-aliens.org/. Accessed 22 Oct 2015; IMPASSE – Environmental impacts of alien spe- Grandidierella japonica Stephensen, 1938: Nagata cies in aquaculture. http://www2.hull.ac.uk/science/biologi- (1960); Chapman and Dorman (1975); Myers (1981); cal_sciences/research/hifi/impasse.aspx. Accessed 22 Oct Greenstein and Tiefenthaler (1997); Cohen et al. (1998); 2015) assess its absence from the Mediterranean. Smith et al. (1999); Cohen (2002); Ashelby (2006); Table 1 Main environmental characteristics of the ten sampling station during the sampling campaign of January 2015 (OM, organic matter as percentage of dry weight; RPDL, depth of redox potential discontinuity layer) Lat Long Depth O2 Temp Sal RPDL OM DD DD m mg/L °C PSU mm %DW C1 44°49.061' N 12°19.395' E 1.7 6.6 6.8 34 1 6.80 C2 44°47.783' N 12°19.422' E 1.5 4.7 6.7 32 0 1.03 C3 44°47.717' N 12°20.620' E 1.5 5.8 6.8 35 0 4.49 C4 44°47.599' N 12°21.616' E 1.2 5.8 6.2 35 0.5 3.37 C5 44°47.435' N 12°22.328' E 0.7 6.3 5.4 35 0.5 4.87 P1 44°49.758' N 12°18.105' E 1.7 7.2 6.8 32 0.5 4.77 P2 44°48.676' N 12°20.748' E 1.3 6.5 5 34 1 5.26 P3 44°48.353' N 12°21.223' E 1 6.7 5.2 34 1 6.46 P4 44°48.079' N 12°21.615 E 1 6.7 5.1 34 1 4.42 P5 44°47.793' N 12°22.177' E 0.5 6.5 4.9 34 0.5 4.80 Munari et al. Marine Biodiversity Records (2016) 9:12 Page 3 of 8 Fig. 1 Grandidierella japonica Stephensen, 1938: (a) adult male; (b) adult female. Scale bars: A-B, 1mm Okolodkov et al. (2007); Ariyama (2007); Jourde et al. in female (juvenile from 1.9mm), excluding antennae. (2013); Lavesque et al. (2014). All male specimens lacking antennae, with the exception From samples gathered in the Sacca di Goro on 13 of 1 with Antenna 1 (Fig. 1a) greater than one-half body January 2015, we collected 197 specimens of Grandidier- length and flagellum with 20 articles; article 1 of ped- ella japonica, 56 out of these were in good condition. uncle with ventral spines (Fig. 2a). Specimens shows Among these we examined the best preserved specimens: marked sexual dimorphism, particularly in the size and 8 adult males (Fig. 1a), 12 females (Fig. 1b), and 4 undiffer- shape of the gnathopod 1. Male gnathopod 1 (Fig. 2b-d) entiated juveniles. None of the specimens was complete; all massive, carpochelate; articles 2 and 5 greatly enlarged; were missing their antennae with the exception of two article 5 with three distal posterior teeth (Fig. 2b), one specimens; most of them were also missing pereopods 3-7. tooth enlarged, forming a thumb, one tooth double The body of adult specimens was mottled grey to grey (Fig.

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