Research Article
Print
Research Article
The world-wide invader Deltamysis holmquistae expanded to the East Atlantic and Diamysis lagunaris to the North Sea (Crustacea, Mysida)
expand article infoKarl J. Wittmann‡, Ton van Haaren§, Rianna Vlierboom§
‡ Medical University of Vienna, Vienna, Austria
§ Eurofins AquaSense, Amsterdam-Duivendrecht, Netherlands

Corresponding author: Karl J. Wittmann ( karl.wittmann@meduniwien.ac.at )

Academic editor: Elizabeth Joanne Cottier-Cook
© 2024 Karl J. Wittmann, Ton van Haaren, Rianna Vlierboom.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Wittmann KJ, van Haaren T, Vlierboom R (2024) The world-wide invader Deltamysis holmquistae expanded to the East Atlantic and Diamysis lagunaris to the North Sea (Crustacea, Mysida). Aquatic Invasions 19(4): 413-429. https://doi.org/10.3391/ai.2024.19.4.141425
Open Access

Abstract

In October 2023 and April 2024, ecological monitoring was undertaken in brackish waters of the North Sea Canal, a major shipping route linking the Port of Amsterdam to the North Sea. Amongst the macrobenthic samples, four endemic and three non-native mysid species were recorded, two of the latter for the first time in this locality. This concerns the now globally distributed Deltamysis holmquistae, and the Mediterranean Diamysis lagunaris. Based on the spatial context, these specimens are highly likely to have been introduced through human-mediated transport, with shipping providing the most obvious entry path into the North Sea Canal. Both species were found in fully artificial and in restored near-natural habitats, highlighting their versatility as invasive species. Pictorial descriptions and complete keys for both species are included in order to facilitate future assessments of potential range expansions.

Key words

Introduced species, keys to species, re-naturalized habitats, transoceanic expansion, worldwide invasive species

Introduction

The North Sea Canal (NSC) at the NE-Atlantic coast of the Netherlands is known to contain a high number of non-native species (Verleye et al. 2020) because it is a major route for inland and maritime shipping. The canal itself, completed in 1876, is mostly artificial, but in recent years some parts have been designed as “nature friendly banks” with the aim of encouraging native biodiversity (Besteman 2006). Native as well as non-native mysid species have been found in both the artificial main channel and in these restored habitats. Duijts et al. (2021) recorded the mysid Neomysis americana (S.I. Smith, 1873) in the NSC in 2021, a Western Atlantic species first reported in European waters by Wittmann et al. (2012), namely around the island of Schiermonnikoog in the Dutch Wadden Sea. This species has been found in estuaries along the NE-Atlantic coast of Europe including the Netherlands, Belgium, and France (Pezy et al. 2018; Brind’Amour et al. 2021; Kruijt et al. 2021; Soors et al. 2022; Droual et al. 2024) and has therefore become well established in European waters. Two additional non-native mysids were discovered in the NSC during surveys taken in October 2023 and April 2024, highlighting the role of shipping routes for the dispersal of mysids, as previously known from other crustacean taxa (Williams et al. 1988; Wolff 1999; Bij de Vaate et al. 2002; Wittmann 2005; U.S. Geological Survey 2022).

Material and methods

Study area

In the frame of ecological monitoring, benthic samples were taken in estuarine waters along the entire length of the North Sea Canal (NSC), a heavily trafficked shipping route from the Port of Amsterdam to the North Sea. The canal (Fig. 1) has a total length of 28 km, depths of 8–23 m, a bottom width of 170 m, and a surface width of 270 m. The NSC also includes ten side canals and several ports. The banks of the main canal are artificial, mainly consisting of rubble and sheet piling, and the bottom of the canal is primarily silt with some shell fragments and empty tube worm casings. In addition to sampling the main canal, side canals and ports with mostly stony banks, some samples were taken along the canal at re-naturalized habitats termed ‘NVO’ as an acronym for “Natuur vriendelijke oever”, translated as ‘Nature Friendly Bank’. These habitats are open and connected to the main canal. They are shallower (1 m), dominated by soft sediment, and bordered by reeds. Only the banks of Assendelft and Spaarnwoude along canal-kms 8–10 were specifically designed as NVOs. The banks of Zijkanaal C at km 10, Kleine Noorder IJplas at km 19.5, and Hargergat in Zeeburg at km 28 are not entirely covered by stones but also have some reed-vegetation, making them ‘nature friendly’ (Fig. 1). Salinities were measured by Rijkswaterstaat along the main canal in 2023–2024 simultaneously with our sampling. Salinities in 1 m depth were 7 psu at canal-km 6 and 6 psu at km 12; bottom salinities in 15–20 m depth were 21 psu at km 6 and 19 psu at km 12 (data recalculated from Rijkswaterstaat, with permission).

Figure 1. 

Map of the NSC area with records of three introduced mysid species taken in 2023/24. Coinciding points slightly displaced. Kilometre markers 1–28 are given as series of dots indicating the distance from the North Sea. Map by Lotte Lubos, modified.

Methods and definitions

In October 2023 and April 2024, the NSC was sampled for invertebrates using diverse techniques, three of which yielded mysids: a boxcorer of 0.057 m2 and a van Veen-grab of 0.025 m2 in the deeper main canal, and a pond net on the banks and in the re-naturalized habitats. The samples were preserved in 96% ethanol. Laboratory methods and definitions used for examination and description of mysid species are as in Wittmann (2024). Body length (BL) was measured from tip of rostrum to terminal margin of telson without spines. Note that expansion on slides makes the carapace appear broader (but not longer) with respect to the shape in loco. Photos and drawings of sex-specific features are labelled by symbols for females or males. The absence of such labels implies absent or unapparent sex-specific differences. Artificial green colouring of microphotographs serves to increase the contrast in the online version.

The term ‘introduced’ is used for any non-native species in the canal, ‘invasive’ for introduced species with populations already established (repeatedly found) here or elsewhere far from the natural range.

Results

The 2023/24 survey in the NSC (Fig. 1) yielded four mysid species native in the North Sea and three introduced species, throughout in brackish water. The native Neomysis integer (Leach, 1814) [i.e. not N. americana (S.I. Smith, 1873)] occurred at canal-km 9.5, 10, 19.5, and 28, Mesopodopsis slabberi (Van Beneden, 1861) at km 9.5 and 19.5, Schistomysis kervillei (G.O. Sars, 1885) at km 11, and S. spiritus (Norman, 1860) at km 14. Among the introduced species, the Ponto-Caspian invader Limnomysis benedeni Czerniavsky, 1882, occurred at km 10, 19.5, and 28; the here first recorded invasive species Deltamysis holmquistae Bowman & Orsi, 1992, at km 6, 9.5, and 11, the introduced species Diamysis lagunaris Ariani and Wittmann (2000), native in the Mediterranean, at km 9.5, 10, and 19.5. Five species, namely Deltamysis holmquistae, Diamysis lagunaris, L. benedeni, N. integer, and M. slabberi, occurred at NVOs but also in the main canal (Fig. 1), whereas both Schistomysis species occurred only in more saline waters at the bottom of the main canal. Judging from this comparatively small number of species, there was no visible contingency between the native status of the species and the near-natural status of the habitat. The West Atlantic invader N. americana was recorded in 2021 by Duijts et al. (2021) in the Side Canal H (km 18.5), but the present investigation did not yield any specimen in the NSC.

Genus Deltamysis Bowman & Orsi, 1992

Deltamysis holmquistae Bowman & Orsi, 1992

Figs 2, 3, 4

Material examined

North Sea Canal • 1 ♂ ad. with BL 3.4 mm (most thoracopods broken, on slides); Spaarnwoude, loc. code NVO-SW; 52.4367°N, 4.7057°E; 16 Oct. 2023; T. van Haaren leg.; canal-km 9.5, brackish water, shallow (<1 m), sandy bottom, pond net; sample code 2023EASC00024 • 1 ♀ ad., 3.7 mm, with empty marsupium, in 2 parts, 1 ♀ subad., 3.8 mm (in vial); canal-km 11, Nauerna, loc. code NZK-11-O; 52.4306°N, 4.7368°E; 4 Oct. 2023; R. Vlierboom and S. Honcoop leg.; depth 4 m, boxcorer; sample code 2023EASC00003.03 • 1 ♀ ad., 3.8 mm, with empty marsupium, 1 ♂ ad., 3.1 mm, 1 ♀ subad., 3.4 mm, 1 imm., 2.8 mm, in 2 parts (in vial); canal-km 6, Velzen, loc. code NZK-06-O; 52.4541°N, 4.6749°E; 5 Oct. 2023; R. Vlierboom and S. Honcoop leg.; depth 6 m, van Veen-grab; sample code 2023EASC00001.03.

Note

The present specimens fit well to the morphological scheme first published by Bowman and Orsi (1992) and revised by Scripter et al. (2020) and Daneliya (2023). Cornea dorsoventrally compressed by a factor of 1.2–1.5. Exopod of maxilla (Fig. 3E) with 2–4 barbed setae on distal half of lateral margin, proximal half bare. Statoliths composed of fluorite. Figs 2, 3 provide the essential details for determination at species level. In addition, a dichotomous textual key to the four here acknowledged species of the genus Deltamysis Bowman & Orsi, 1992, is given below.

Figure 2. 

Deltamysis holmquistae from the NSC; ♂ ad., 3.4 mm A ♂ in toto, lateral, thoracopods 2–8 broken B cephalothorax, dorsal C cephalic region, ventral D penis (pe) with spermatozoa (sz) and thoracic sternites 4–8, ventral; penis forced tightly against the sternites by the cover glass E telson, dorsal. A–C, E objects artificially separated from background. Micrographs by K.J. Wittmann.

Figure 3. 

Deltamysis holmquistae from the NSC; ♂ ad. with BL 3.4 mm (A–E, G–I) and ♀ subad., also 3.4 mm (F). A carapace expanded on slide, pores indicated as dots are not to scale, dorsal B left male antennular trunk, dorsal C antenna, setae of antennal scale omitted, ventral D mandibular palp E palp and exopod of maxilla, rostral F right thoracopod 2, rostral G right male pleopod 2, lateral = rostral H right male pleopod 4, lateral I uropods, setae omitted, ventral.

Figure 4. 

Worldwide distribution of Deltamysis holmquistae. Data from Bowman and Orsi (1992), Scripter et al. (2020), Daneliya (2023), and present contribution.

Distribution

Bowman and Orsi (1992) first described this species from the San Joaquin Estuary at the coast of California. Later the species was found in shallow mixoeuhaline to anhaline waters of Texas, Florida, and Australia (Scripter et al. 2020; Daneliya 2023). From their redescription based on Florida and Texas materials, Scripter et al. (2020) concluded that the mysid Kochimysis pillaii Panampunnayil & Biju, 2007, from the SW-coast of India is to be considered a junior subjective synonym of D. holmquistae. The published records of D. holmquistae together with the present records from the E-Atlantic fit together to a circumtropical distribution between 37°S and 52°N (Fig. 4). Potential regions of origin of this invasive species are considered in the ‘Discussion’.

Key to the species in the genus Deltamysis

Modified from Daneliya 2023.

1 Telson roughly trapezoid with continuously rounded, convex terminal margin; telson length 0.9–1.3 times maximum width, spines only on distal 10–20% telson length; paramedian pair of spines longest, neighbouring disto-lateral spines continuously decreasing in length laterally. Songkhla Lagoon system, southern Thailand D. songkhlaensis (Yolanda, Sawamoto & Lheknim, 2019)
– Telson trapezoid with truncate terminal margin with or without (Fig. 2E) mid-terminal indentation, disto-lateral edges rounded; spines only on distal 20–35% telson length, paramedian spines (Fig. 2E) or laminae clearly shorter than neighbouring spines 2
2 Telson elongate trapezoid with small mid-terminal indentation; telson length 1.5–1.6 times maximum width; exopod of maxilla densely setose almost all along lateral margin. Australia: Northern Territory, Channel Island D. nana (Murano, 1998)
– Telson trapezoid with or without (Fig. 2E) mid-terminal indentation; telson length 1.1–1.4 times maximum width; exopod of maxilla (Fig. 3E) with 0–5 barbed setae on distal half of lateral margin, proximal half bare 3
3 Eyes large (Fig. 2A, B); cornea calotte-shaped (Fig. 1B) in dorsal view, ovoid (Fig. 1A) in lateral view, maximum length of the ovoid exceeds length of terminal segment of antennular trunk; telson (Fig. 2E) trapezoid with rounded disto-lateral edges; terminal margin transverse, not emarginated, with 2–3 medium-sized paramedian spines flanked by 1–2 pairs of larger spines; subterminal lateral spines longer than preceding lateral spines. Estuarine circumtropical invader between 37°S and 52°N, probably native in the Indo-Pacific D. holmquistae Bowman & Orsi, 1992
– Eyes large; maximum length of the ovoid cornea (lateral aspect) shorter than length of terminal segment of antennular trunk; telson roughly trapezoid with weakly emarginated terminal margin; shallow indentation all along furnished with seven short laminae; disto-lateral edges each with one large spine flanking the cleft; subterminal lateral spines shorter than preceding lateral spines. Australia, New South Wales: Clarence River mouth, Yamba D. lowryi Daneliya, 2023

Genus Diamysis Czerniavsky, 1882

Diamysis lagunaris Ariani & Wittmann, 2000

Figs 5, 6, 7

Material examined

North Sea Canal • 11 ♀♀ ad. with BL 5.7–7.0 mm, 2 ♂♂ ad., 5.7–6.0 mm, 3 subad., 12 imm. (damaged, in vial), 1 ♂ ad., 6.2 mm (most thoracopods broken, on slide); Spaarnwoude, loc. code NVO-SW; 52.4367°N, 4.7057°E; 16 Oct. 2023; T. van Haaren leg.; canal-km 9.5, shallow (<1 m), sandy bottom, pond net; sample code 2023EASC00024 • 2 ♀♀ ad., 9.2–10.2 mm, 1 ♂ ad., 7.2 mm, 1 imm., 3 juv. (well-preserved, in vial); 23 Apr. 2024; T. van Haaren and J.I. Knetsch leg.; sample code 2024EASD00029; remaining sampling data as for preceding • 1 ♂ ad., 6.1 mm (most thoracopods broken, in vial); Buitenhuizen, Assendelft, loc. code NVO-AD; 52.4363°N, 4.7178°E; 10 Oct. 2023; T. van Haaren leg.; canal-km 10, shallow (<1 m), sandy bottom, pond net; sample code 2023EASC00025 • 2 ♂♂ ad., 7.0–7.3 mm, 1 ♀, 9.3 mm, carrying 27 damaged nauplioid larvae (adults well-preserved, on slides); 22 Apr. 2024; T. van Haaren and J.I. Knetsch leg.; sample code 2024EASD00030; remaining sampling data as for preceding • 1 spec. with head missing; Kleine N’IJplas west side, loc. code KNIJP2-Ow, 52.4179°N, 4.8632°E; 18 Apr. 2024; T. van Haaren leg.; canal-km 19.5, shallow (<1 m), pond net; sample code 2024EASD00033 • 1 spec.; Kleine N’IJplas south side, loc. code KNIJP-Oz, 52.41711°N, 4.86044°E; sample code 2024EASD00028; remaining sampling data as for preceding.

Diagnosis

Modified from Ariani and Wittmann (2000) in order to include the large-sized specimens of the NSC (size comparison given below). Forward directed disto-mesial lobe (arrow in Fig. 6B) above inner flagellum of male antennular trunk less than half as long as basal width of flagellum. Antennula with well-developed appendix masculina (Fig. 6B). Cornea occupies 50–70% of the length of eyestalk (Fig. 5E). Eyestalks with strongly developed fenestra paracornealis (arrow in Fig. 5E), even if not always well visible in poorly pigmented stalks. Carapace (Fig. 6A) without fringes in both sexes. Distal segment of maxillary palp with 5–25 denticles (Fig. 6C). Basal segment of thoracic exopods 1–8 with outer corner mostly spiniform (Fig. 6E), though less frequently rounded in exopods 5–8. Carpopropodus of thoracic endopods 3–8 with 3–2 (4), 2–3, 2–3, 2–3, 2, and 2–3 segments (Fig. 6D, E); tarsus comparatively slender with slender styliform claw. Carpopropodus of endopod 3 (Fig. 6D) with basal segment 2.9–3.7 times as long as its maximum width. Basal segment not longer than remaining segments combined in carpopropodites 3 with more than two (Fig. 6D) segments. Penes (Fig. 6F) with all or with most setae smooth, with few barbed setae, if any. Exopod of male pleopod 4 is 2-segmented (Fig. 6H), basal segment distally with a smooth seta, occasionally accompanied by a small, barbed seta. Scutellum paracaudale (Fig. 5D) well-rounded to biconvex with rounded to acute edge. Statoliths composed of vaterite. Telson (Fig. 5F) trapezoid to subtriangular, length 1.1–1.5 times maximum width; maximum width 1.8–2.7 times that at apex. Each lateral margin all along with 6–16 spines decreasing in length from basis to about half telson length and from there increasing in length distally. Terminal margin of telson with pair of large disto-lateral spines flanking a deep cleft penetrating 11–19% telson length; cleft with distinctly convex lateral margins forming an angle of < 90°; margins all along armed with laminae. Telson with totals of 14–34 spines and 9–26 laminae.

Figure 5. 

Diamysis lagunaris from the NSC; ♂ ad., 7.3 mm (A), ♀♀ ad., 6.9 mm (B), 6.5 mm (C), 6.6 mm (D), 6 mm (E) and ♂ ad., 6.2 mm (F). A ♂ in toto, lateral B ♀ in toto, most thoracopods broken, lateral C ♀ in toto, left antennula and antenna broken, dorsal D caudal margin of pleomere 6 with anal bulge (ab) and basis of endopod of uropod (eu), dashed line enhances contour of scutellum paracaudale (sc), lateral E right eye, arrow points to fenestra paracornealis, dorsal F telson, dorsal. A–C, E–F objects artificially separated from background. Micrographs by K.J. Wittmann

Figure 6. 

Diamysis lagunaris from the NSC; ♀ ad., 6 mm (A), ♂♂ ad., 6.2 mm (B–D, F), 7.3 mm (E), 7.0 mm (G), 6 mm (H) and ♀ ad., 9.3 mm (I). A carapace expanded on slide, pores indicated as dots are not to scale, dorsal B left male antennular trunk, dorsal, arrow points to disto-mesial lobe C maxillary palp, setae omitted D tarsus of thoracic endopod 3 E thoracopod 6, caudal F penis G male pleopod 3, frontal = lateral H male pleopod 4 in a smaller specimen compared with (G), most setae broken, frontal I uropods, setae omitted, ventral.

Note

Body length of adults is 6–10 mm in females (n = 14) and 6–7 mm in males (n = 6) in brackish waters of the NSC at 52°N in the North Sea versus 5–7 mm in females (n = 1236) and 4–6 mm in males (n = 617) at the type locality in the mixoeuhaline to weakly metahaline lagoon Lago di Caprolace at 41°N in the Tyrrhenian Sea (Ariani and Wittmann 2000). On the average larger adult sizes in colder climates is a normal feature in Mysidae (Wittmann 1984). Fenestra paracornealis with 1–5 free ommatidia in series along the margin of the cornea but not integrated in the cornea (arrow in Fig. 5E). Figs 5, 6 show the essential details of the present specimens for determination at species level. In addition, a key to the currently acknowledged 14 species plus two non-nominotypical subspecies of the genus Diamysis is given below.

Distribution

Type locality of D. lagunaris is the Lago di Caprolace at the Lazio coast, Tyrrhenian Sea. Other published Mediterranean records cover Aegean, Sardinian and Ligurian seas, the Strait of Messina, Gulf of Lion, and the Baleares (Ariani and Wittmann 2000; Wittmann and Ariani 2012). Published NE-Atlantic records extend from the Gulf of Cádiz to the south and west coasts of Portugal (as D. bahirensis in Drake et al. 1997; Cunha et al. 2000; San Vicente and Munilla 2000; as D. lagunaris in Wittmann and Ariani 2012). The present records extend the known Atlantic distribution northward to the Dutch coast of the North Sea (Fig. 7). Potential native versus introduced status of populations is considered in the ‘Discussion’.

Figure 7. 

Distribution of Diamysis lagunaris. Modified and updated from Wittmann and Ariani (2012).

The normal salinity range is 14–49 psu. Only two positive samples were previously known from oligohaline waters (S = 2–3 psu), namely from different stations in the Rhône Delta on the Mediterranean coast of France (Wittmann and Ariani 2012). The records in the re-naturalized sites of the NSC were made before (10–16 Oct. 2023) as well as after (22–23 Apr. 2024) 5 Jan. 2024 when the near-surface salinity was < 2 psu. This makes it plausible but not definite that the mysids were exposed to and had survived oligohaline conditions in winter. Among the currently acknowledged 14 species of Diamysis, ten species are Mediterranean endemics (among these, D. cymodoceae is also found in the Marmora Sea and the southern Black Sea; D. lagunaris also found in the NE-Atlantic) as well as one each from the Pontian, Ponto-Caspian, Caspian, and W-Indian Ocean plus Red Sea.

Key to the species and subspecies in the genus Diamysis

Modified and updated from Wittmann and Ariani 2012.

l Distal segment of maxillary palpus without denticles. Exopod of male pleopod 4 with only one modified, strong seta at tip. Basal segment of thoracic exopods with outer corner rounded. All pereiopods with 2-segmented, slender carpopropodus; claw long and slender. W-Indian Ocean and Red Sea, marine coastal D. frontieri H. Nouvel, 1965
– Distal segment of maxillary palpus with distinct denticles (Fig. 6C). Exopod of male pleopod 4 with 1–3 (rarely 4) setae 2
2 Exopod of male pleopod 4 with only one modified, strong seta at tip (Fig. 6H). Thoracic endopods 3 and 4 with 2- to 3-segmented, stout carpopropodus; carpopropodus 3 shorter than 5 times its maximum width; claw short and strong. This carpopropodus with basal segment longer than remaining segments combined 3
– Exopod of male pleopod 4 with a large seta (and rarely an additional, minute seta) at tip, and 1–2 smaller setae at penultimate segment (Fig. 6H). Thoracic endopods 3 and 4 with 2- to 4-segmented, slender to moderately stout carpopropodus; carpopropodus 3 longer than 5 times its maximum width (Fig. 6D); thoracic endopods generally with long and slender claw (strong claw only in endopod 7 (6) of D. bacescui) 4
3 Eyes short and thick, cornea about 80–100% the length of eyestalk in dorsal view. Telson subtriangular, maximum width about 2.7 times that at apex; cleft narrow, forming a distinct incision, armed with about six laminae. Caspian Sea, coastal D. pusilla (G.O. Sars, 1907)
– Cornea 70–80% the length of eyestalk. Telson subquadrangular, maximum width 1.7–2.0 times that at apex; cleft wide and extremely shallow, armed with 20–31 laminae. Carapace without fringes in both sexes. Lakes and river systems of the Caspian, Black, and Azov seas, freshwater D. pengoi (Czerniavsky, 1882)
4 Cornea small, about 40% the length of eyestalk. Exopod of male pleopod 4 more often 3-segmented than 2-segmented. Carpopropodus of 3rd thoracic endopod 3–(4)-segmented; if 3-segmented with basal segment longer than remaining segments combined. Carapace without fringes in both sexes. Brackish-water dolinas at the Ionian coast of Apulia (southern Italy), in part subterranean D. camassai Ariani & Wittmann, 2002
– Eyes normal. Exopod of male pleopod 4 usually 2-segmented, rarely 3-segmented. Carpopropodus of thoracic endopod 3 is 2- to 4-segmented; if more than 2-segmented, with basal segment not longer than remaining segments combined (Fig. 6E). Carapace with or without fringes 5
5 Basal segment of thoracic exopods with outer corner spiniform (Fig. 6E) or occasionally rounded in some of the posterior exopods. Thoracic endopods 4–8 with 3- or 2-segmented carpopropodus 8
– Basal segment of thoracic exopods with outer corner rounded or occasionally spiniform in some of the anterior exopods. Thoracic endopods 5–8 exclusively with 2-segmented carpopropodus (Fig. 6E); endopod 4 with 2-segmented or rarely 3-segmented carpopropodus 6
6 Scutellum paracaudale produced into a large spiniform process. Carapace lined by small fringes along posterior margin in males, smooth in females. Appendix masculina 110–200% the length of terminal segment of antennular peduncle. SW-Mediterranean plus southern and eastern coasts of Sicily, poly- to euhaline lagoons, also marine coastal D. bahirensis (G.O. Sars, 1877)
– Scutellum paracaudale relatively short, terminally rounded (Fig. 5D) or pointed. Carapace without fringes in both sexes (Fig. 6A). Appendix masculina 80–120% the length of terminal segment of antennular peduncle. Coastal waters of the Levantine Sea 7
7 Cornea small, 40–60% the length of eyestalk in dorsal view. Appendix masculina pointing obliquely backwards; this appendix is only 80–90% the length of terminal segment of antennular peduncle. Telson with lateral margins straight, maximum width 2.2–2.6 that at apex. Northern coast of Sinai, metahaline lagoon D. sirbonica Almeida Prado-Por, 1981
– Cornea large, 70–90% the length of eyestalk. Appendix masculina pointing obliquely forwards; this appendix 90–120% the length of terminal segment of antennular peduncle. Telson with lateral margins slightly but distinctly sinusoid, maximum width 2.0–2.3 that at apex. Mediterranean coast of Israel, freshwater to oligohaline stream D. hebraica Almeida Prado-Por, 1981
8 Thoracic endopod 7 and less distinctly also endopod 6 with stout carpus and strong claw, well contrasting with remaining pereiopods. Carapace with small fringes in (para)median position in males, but without fringes in females. Telson subtriangular to subquadrangular, apical cleft with 7–15 laminae. Mediterranean (Tyrrhenian, Adriatic, Aegean, and Levantine seas), marine coastal; most frequently in Posidonia beds D. bacescui Wittmann & Ariani, 1998
– All pereiopods with normal carpopropodus and slender, styliform claw. Telson subquadrangular to subtriangular; its apical cleft with 8–35 laminae (Fig. 5F; numbers differ between individuals and between taxa) 9
9 Eyestalks normal; fenestra paracornealis poorly developed, mostly missing. Scutellum paracaudale subtriangular, with acute or rounded apex 11
– Eyestalks dorsally with well-developed fenestra paracornealis (Fig. 5E), even if not always well visible in poorly pigmented eyestalks. Scutellum paracaudale (Fig. 5D) well rounded or biconvex with rounded to acute apex. Carapace without fringes in both sexes (Fig. 6A). Thoracic endopods 5–7 with 2-segmented carpopropodus (Fig. 6E) 10
10 Apical cleft of telson penetrates 11–19% telson length (Fig. 5F); cleft with distinctly convex lateral margins forming an angle of < 90°. Forward directed disto-mesial lobe (arrow in Fig. 6B) above inner flagellum of male antennular trunk less than half as long as basal width of flagellum. Penes with all or with most setae smooth (Fig. 6F), with few barbed setae, if any. W- and E-Mediterranean, NE-Atlantic coasts from the Gulf of Cádiz to just recently the North Sea (Fig. 7); in oligo- to metahaline waters, mainly in poly- to mixoeuhaline lagoons, also coastal marine D. lagunaris Ariani & Wittmann, 2000
– Apical cleft of telson penetrates only 7–12% telson length; cleft with almost straight lateral margins forming an angle of 110–150°. Forward directed disto-mesial lobe above inner flagellum of male antennular trunk half as long as basal width of flagellum. Penes with barbed setae only. So far known only from the freshwater Lake Scutari close to the SE-coast of the Adriatic Sea (the lake lies on the border of Albania and Montenegro) D. lacustris Băcescu, 1940
11 Carapace with shallow to inconspicuous, mid-dorsal posterior emargination. Male carapace without fringes, or in certain taxa with small fringes in (para)median position; no fringes at all in females. Thoracic endopods 4–7 with 2- or 3-segmented carpopropodus. Appendix masculina 80–120% the length of terminal segment of antennular peduncle (as in Fig. 6B) 12
– Carapace with deep posterior emargination. Posterior half of male carapace furry due to relatively large fringes on both sides, but no fringes in median position; no fringes in females. Thoracic endopods 4–7 with 2-segmented carpopropodus. Appendix masculina 100–200% the length of terminal segment of antennular peduncle. E-Mediterranean (Adriatic, Ionian, and Aegean seas), Sea of Marmora, and SW-Black Sea; mainly in marine vegetation stands, also in meso- to metahaline estuaries and lagoons D. cymodoceae Wittmann & Ariani, 2012
12 Carapace with fringes in males, without fringes in females 15
– Carapace without fringes in both sexes (Fig. 6A) 13
13 Thoracic endopods 3–8 with distally smooth paradactylary setae in both sexes. Thoracic endopod 5 with 3-segmented carpopropodus. Exopod of male pleopod 4 is 2-segmented, with only one (more or less distinctly) barbed seta at basal segment. Black and Azov seas, coastal, brackish lagoons D. mecznikowi (Czerniavsky, 1882)
– Thoracic endopod 3 and often also endopod 8 with at least one among the four paradactylary setae distally pectinate in females, smooth or pectinate in males. Endopod 5 with 2- or 3-segmented carpopropodus. Exopod of male pleopod 4 usually 2-segmented, with smooth seta on basal segment (as in Fig. 6H); in certain populations occasionally with an additional barbed seta, or with additional segment. E-Mediterranean, D. mesohalobia Ariani & Wittmann, 2000 (3 subspecies) 14
14 Thoracic endopods 3–8 relatively short; endopod 8, when stretched anteriorly, extending to basis of endopod 1 or up to mandibles. Endopods 3–8 stout to moderately slender; endopod 6 is 3.9–6.8 times as long as wide. Endopod 5 with 3- or less frequently 2-segmented carpopropodus. Exopod of male pleopod 4 is 2-segmented, with only one smooth seta on basal segment (as in Fig. 6H). Adriatic, Aegean, and Levantine seas, in mesohaline karstic springs and in mesohaline to (mixo)-euhaline lagoons and estuaries D. mesohalobia mesohalobia Ariani & Wittmann, 2000
– Thoracic endopods 3–8 relatively long; endopod 8, when stretched anteriorly, extending up to the labrum or even the eyes. Endopods 3–8 slender; endopod 6 is 5.6–9.1 times as long as wide. Endopod 5 with 2- or rarely 3-segmented carpopropodus. Exopod of male pleopod 4 normally 2-segmented, with smooth seta at basal segment; or occasionally 3-segmented in large males, with distally barbed seta at median segment. Adriatic and Ionian seas, in marine embayments and in mesohaline to mixoeuhaline lagoons and estuaries; also known from one oligohaline spring D. mesohalobia gracilipes Ariani & Wittmann, 2000
15 Carapace of males with numerous small fringes in paramedian position and in a traverse row shortly in front of the posterior margin. Thoracic endopods 3–8 of intermediate length; endopod 8, when stretched anteriorly, extending to maxillae or at most to labrum. Endopods 3–8 stout to slender; endopod 6 is 4.5–7.9 times as long as wide. Thoracic endopod 5 with 2- or less frequently 3-segmented carpopropodus. Exopod of male pleopod 4 is 2-segmented, with smooth seta and occasionally an additional barbed seta on basal segment. Adriatic, Ionian, and Marmora seas, mainly in oligo- to metahaline lagoons (including polyhaline open coasts of the Sea of Marmora) and oligo- to mesohaline estuaries D. mesohalobia heterandra Ariani & Wittmann, 2000
– Carapace of males with numerous small fringes in paramedian position, no fringes near posterior margin of carapace. Thoracic endopods 3 and 8 with paradactylary setae smooth or pectinate in both sexes. Thoracic endopod 5 with 2- or 3-segmented carpopropodus. In tributaries of the N-Adriatic Sea, up to 16 m altitude, mostly in freshwater, also oligohaline, rarely mesohaline D. fluviatilis Wittmann & Ariani, 2012

Discussion

Range expansion of Deltamysis holmquistae

Upon first description of D. holmquistae from the coast of California, Bowman and Orsi (1992) discussed that this species may have been introduced into the E-Pacific but, at that time, they did not know the possible origin. Scripter et al. (2020) reported findings from Florida and Texas and included materials from southern India by synonymization of Kochimysis pillaii Panampunnayil & Biju, 2010. Scripter et al. (2020) proposed that the Florida and Texas populations may have been introduced through human-mediated means, likely due to maritime commerce. They discussed a N-Indian Ocean or NW-Pacific origin, but there was some uncertainty. Daneliya (2023) presented the first records for Australia and argued that this species could be originally Indo-Pacific and introduced in Pacific and Atlantic waters of North America. With the present first records (Fig. 4) from the E-Atlantic, a circumtropical distribution is now confirmed for this strongly expansive species, covering tropical to cold temperate waters of the Atlantic, Indian Ocean, and Pacific. Apart from its role as invasive species, no direct negative effects on the environment have been documented so far.

Range expansion of Diamysis lagunaris

Diamysis lagunaris was first described by Wittmann and Ariani (2000) from shallow waters in poly- to metahaline lagoons and in marine coastal environments of the W-Mediterranean. In the same year, Cunha et al. (2000) reported this species as D. bahirensis (sensu lato) from an oligohaline to mixoeuhaline canal of the lagoon Ria de Aveiro at the coast of Portugal, and proposed that this species has possibly reached the NE-Atlantic coast by an anthropogenic transfer from W-Mediterranean lagoons. Wittmann and Ariani (2012) added records from Crete and the Baleares, suggesting that D. lagunaris shows a high expansion potential, as it is capable of crossing small sea basins. They also demonstrated a chain of records (Fig. 7) from the Mediterranean coast of France around the Iberian Peninsula to the coast of Portugal through new sampling and the revision of previously published species assignments (Drake et al. 1997; Cunha et al. 2000; San Vicente and Munilla 2000). Based on this evidence, they did not exclude a native status of the NE-Atlantic populations. The new records in the NSC are more than 2500 km away from the nearest published record in Portugal (as measured along the coast), which is more suggestive of an introduction through anthropogenic influences than it is of a natural range expansion.

Conclusion

The North Sea Canal is home to a large number of non-native species, and new introductions are continually reported. Shipping has facilitated the transport of many of these, including the two newly reported mysids described herein.

Author Contribution

Sampling, sorting and initial identification of samples was conducted by TvH and RV. Definitive species identification of mysids was undertaken by KJW. Figures, keys, and most of the writing were completed by TvH and KJW. All authors contributed to the editing, formatting, and finalising of the manuscript.

Acknowledgements

The authors thank the colleagues of Eurofins AquaSense who aided with sampling and sorting. Particular thanks are given to Lotte Lubos for her assistance in creating the maps, and Marco Faasse for additional information about certain introduced species. Marco van Wieringen (Rijkswaterstaat West-Nederland Noord) is thanked for his permission to share these findings, additional information regarding the abiotic factors in the NSC. Sincere thanks to the reviewers for their efforts in reviewing our manuscript. We greatly appreciate their valuable comments and suggestions to improve the quality of the manuscript.

References

  • Ariani AP, Wittmann KJ (2000) Interbreeding versus morphological and ecological differentiation in Mediterranean Diamysis (Crustacea, Mysidacea), with description of four new taxa. Hydrobiologia 441: 185–236. https://doi.org/10.1023/A:1017598204238
  • Ariani AP, Wittmann KJ (2002) The transition from an epigean to a hypogean mode of life: morphological and bionomical characteristics of Diamysis camassai sp. nov. (Mysidacea, Mysidae) from brackish-water dolinas in Apulia, SE-Italy. Crustaceana 74 (11): 1241−1265. https://doi.org/10.1163/15685400152885219
  • Bij de Vaate A, Jazdzewski G, Ketelaars HAM, Gollasch S, Van der Velde G (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 59: 1159–1174. https://doi.org/10.1139/F02-098
  • Brind’Amour A, Day L, Cresson P, Vogel C, Chouquet B, Pezy J-P, Dauvin J-Cl, Duhamel S, Le Bris Hervé H (2021) CAPES “CApacité trophique des nourriceries de Poissons de l’Estuaire de Seine”. In: Rapport de recherche du programme Seine-Aval 6, GIP Seine-Aval, Rouen, 70 pp. https://archimer.ifremer.fr/doc/00710/82164/
  • Cunha MR da, Moreira MH, Sorbe J-C (2000) Diamysis bahirensis: a mysid species new to the Portuguese fauna and first record from the west European coast. In: Vaupel Klein JC von, Schram FR (Eds) The Biodiversity Crisis and Crustacea. Crustacean Issues 12, A.A. Balkema, Rotterdam, 139–152.
  • Czerniavsky V (1882) Monographia Mysidarum inprimis Imperii Rossici (marin., lacustr. et fluviatilium). Fasc. 1. Trudy Sankt-Peterburgskago obshchestva estestvoispytatelei 12(2): 1–170. [pls I-IV] http://vliz.be/en/imis?module=ref&refid=71248
  • Droual G, Lécuyer R, Pezy J-P (2024) First observation of the non-indigenous mysid Neomysis americana (S.I. Smith, 1873) in the Loire estuary. BioInvasions Records 13(3): 755–766. https://doi.org/10.3391/bir.2024.13.3.14
  • Murano M (1998) Further study on Australian heteromysids (Crustacea: Mysidacea). The Beagle, Records of the Museums and Art Galleries of the Northern Territory 14: 29–39. https://doi.org/10.5962/p.266450
  • Panampunnayil SU, Biju A (2007) A new genus and species of Heteromysini (Crustacea-Mysidacea) from the backwater of Kochi (Kerala, India). Journal of Natural History 41(29): 1955–1963. https://doi.org/10.1080/00222930701515553
  • Pezy J-P, Raoux A, Timsit O, Dauvin J-C (2018) A rapidly established population of the invader mysid Neomysis americana (S.I. Smith, 1873) in the Seine estuary. Marine Biodiversity 49: 1573–1580. https://doi.org/10.1007/s12526-018-0914-5
  • Sars GO (1877) Nye Bidrag til Kundskaben om Middelhavets Invertebratfauna I. Middelhavets Mysider. Archiv for Mathematik og Naturvidenskaberne 2: 10–119. [pls 1–36] https://doi.org/10.5962/bhl.title.10404
  • Sars GO (1885) Description d’une espèce nouvelle de Mysis. Mysis Kervillei G.-O. Sars. In: Gadeau de Kerville H, Sars GO (eds) , Note sur les Crustacés Schizopdes de l’estuaire de la Seine, suivie la description d’une espèce nouvelle de Mysis, Mysis Kervillei G. -O. Sars. Bulletin de la Société des Amis des Sciences Naturelles de Rouen, ser. 3, 21, 92–98. [pl. V] https://marinespecies.org/traits/aphia.php?p=sourceget&id=9451
  • Sars GO (1907) Mysidae. In: Report of the Caspian expedition 1904. St. -Peterburg 1: 243–313. [pls I–XII]
  • Scripter MJ, Price WW, Heard RW (2020) Redescription of Deltamysis holmquistae Bowman & Orsi, 1992 (Crustacea: Mysida: Mysidae), a mysid species new to the Atlantic Ocean with observations on the taxonomic status of Kochimysis Panampunnayil & Biju, 2007. Zootaxa 4729: 501–518. https://doi.org/10.11646/zootaxa.4729.4.3
  • Soors J, de Beukelaer J, Bezdenjesnji O, Buerms D, Lefranc C, Speybroeck J, Van de Meutter F (2022) Two new alien crustacean invaders Grandidierella japonica (Stephensen, 1938) and Neomysis americana (S.I. Smith, 1873) in Belgium. BioInvasions Records 11(3): 747–757. https://doi.org/10.3391/bir.2022.11.3.16
  • U.S. Geological Survey (2022) United States Register of Introduced and Invasive Species (US-RIIS), all versions: U.S. Geological Survey data release. ScienceBase. https://doi.org/10.5066/P92DN8D8
  • Van Beneden P-J (1861) Recherches sur les crustacés du littoral de Belgique. Mémoires de l’ Académie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique 33: 1–174. [pls I–XXI] https://doi.org/10.3406/marb.1861.3554
  • Williams RJ, Griffith FB, Van der Wal EJ, Kelly J (1988) Cargo vessel ballast water as a vector for the transport of non-natives marine species. Estuarine, Coastal and Shelf Science 26: 409–420. https://doi.org/10.1016/0272-7714(88)90021-2
  • Wittmann KJ (1984) Ecophysiology of marsupial development and reproduction in Mysidacea (Crustacea). Oceanography and Marine Biology. An Annual Review 22: 393–428. https://doi.org/10.1201/9781482267242
  • Wittmann KJ (2005) Anthropogenic dispersal and environmental impact of invasive species of Mysidae (Mysidacea: Crustacea) on a world-wide scale. In: EGU General Assembly 2005, Vienna. Geophysical Research Abstracts 7: 1088.
  • Wittmann KJ (2024) Mysidae (Crustacea: Mysida) from sponges in sublittoral waters of Lizard Island (Indo-Pacific: Coral Sea), with description of Heteromysis kaufersteinae sp. nov., first record of H. domusmaris from nature, and range extension in Anchialina lobata. Crustacean Research 53: 97–111. https://doi.org/10.18353/crustacea.53.0_97
  • Wittmann KJ, Ariani AP (1998) Diamysis bacescui n.sp., a new benthopelagic mysid (Crustacea: Peracarida) from Mediterranean seagrass meadows: description and comments on statolith composition. Travaux du Muséum national d’Histoire naturelle “Grigore Antipa” 40: 35–49. https://www.vliz.be/imisdocs/publications/ocrd/282492.pdf
  • Wittmann KJ, Ariani AP (2012) Diamysis cymodoceae sp. nov. from the Mediterranean, Marmora, and Black Sea basins, with notes on geographical distribution and ecology of the genus (Mysida, Mysidae). Crustaceana 85: 301–332. https://doi.org/10.1163/156854012X623719
  • Wittmann KJ, Vanagt TJ, Faasse MA, Mees J (2012) A new transoceanic invasion ? First records of Neomysis americana (Crustacea: Mysidae) in the East Atlantic. The Open Marine Biology Journal 6: 62–66. https://doi.org/10.2174/1874450801206010062
  • Wolff WJ (1999) Exotic invaders of the meso-oligohaline zone of estuaries in the Netherlands: why are there so many? Helgoländer wissenschaftliche Meeresuntersuchungen 52: 393–400. https://doi.org/10.1007/BF02908913
  • Yolanda R, Sawamoto S, Lheknim V (2019) A new species in the genus Heteromysoides (Crustacea, Mysida, Mysidae) from Songkhla Lagoon, southern Thailand. Zoosystematics and Evolution 95(2): 535–542. https://doi.org/10.3897/zse.95.39214
login to comment