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Research Article
Distribution and species identification in the crustacean isopod genus Dynamene Leach, 1814 along the North East Atlantic-Black Sea axis
expand article infoPedro E. Vieira, Henrique Queiroga, Filipe O. Costa§, David M. Holdich|
‡ Universidade de Aveiro, Aveiro, Portugal
§ Universidade do Minho, Braga, Portugal
| Unaffiliated, Nottingham, United Kingdom
Open Access

Abstract

Sphaeromatid isopods, such as Dynamene, are common and abundant members of the invertebrate fauna of littoral and shallow sublittoral substrates. Six species of Dynamene occur in the northern hemisphere. Only two species exist outside this range, in Australia. The distribution of the various species in the NE Atlantic-Black Sea axis has been controversial due to the difficulty in the identification of the different species. This has led to inaccurate records of their distribution, ultimately generating uncertain or faulty assessments on the biodiversity of these habitats. An update and a clarification about the distribution of this genus is therefore in order. In this study, we describe the distribution of Dynamene species in the light of new records from the NE Atlantic Ocean and its associated islands, and the Mediterranean, Black and Red Seas, and from re-examination of museum and several authors’ personal collections. Based on these observations, we extend the northern and southern limits of D. bidentata (Adams); the western and southern limits of D. magnitorata Holdich; the northern, eastern and western limits of D. edwardsi (Lucas); and the eastern and western limits of D. bifida Torelli. The range of Dynamene tubicauda Holdich is extended, but is still only known from the eastern Mediterranean. We also clarify the synonymy of D. torelliae Holdich with D. bicolor (Rathke), and the occurrence of D. bicolor in the Black Sea. New distribution maps of the six Dynamene species are presented. Illustrated keys to the adult males and females of the northern hemisphere species are provided.

Keywords

Dynamene, Crustacea, Isopoda, Sphaeromatidae, identification, distribution

Introduction

Isopod crustaceans are common and sometimes abundant members of the invertebrate fauna of the littoral and shallow sublittoral habitats of the world’s oceans (Poore and Bruce 2012). Species of the sphaeromatid isopod genus Dynamene Leach, 1814 are typical components of these habitats on coasts of the NE Atlantic Ocean and its islands, and the Mediterranean and Black Seas. Six species are endemic to these provinces (Holdich 1968a, 1970): D. bidentata (Adams, 1800); D. bicolor (Rathke, 1837); D. edwardsi (Lucas, 1849); D. bifida Torelli, 1930; D. magnitorata Holdich, 1968 and D. tubicauda Holdich, 1968. Dynamene torelliae Holdich, 1968 was considered to be synonymous with D. bicolor by Kussakin (1979) and this has been accepted by the current authors. Two additional species occur in, and are endemic to, Australia, but have rarely been recorded: Dynamene ramuscula (Baker, 1908) and Dynamene curalii Holdich and Harrison, 1980. A number of other Dynamene species are incorrectly listed in some databases, e.g., http:/isopods.nhm.org/, Brusca et al. (1995-2004), Myers et al. (2008). Species attributed to the genus Dynamene from the western USA, i.e., D. angulata Richardson, 1901; D. benedicti (Richardson, 1899); D. dilatata Richardson, 1899; D. glabra Richardson, 1899 and D. sheari Hatch, 1947 do not belong to this genus, as adult males do not possess a bidentate process arising from the sixth pereonite (see below), and are considered incertae sedis (http://www.marinespecies.org/). Dynamene tuberculosa Richardson, 1899 from the Aleutian Islands off Alaska is also still listed as such in some databases, but was considered as the female of Paracerceis cordata (Richardson, 1899) by Richardson (1905).

The distribution of the various Dynamene species associated with the NE Atlantic-Black Sea axis was previously examined by Holdich (1968a, 1970). Since then many general community studies have been published reporting the presence of Dynamene throughout its range (e.g., Pereira et al. 2006 in Portugal, Arrontes and Anadón 1990, Arrontes 1991, Viejo 1997, Castelló and Carballo 2001 in Spain, Castellanos et al. 2003 in northern Africa; and Kirkim et al. 2006 in Turkey). In addition, a large number of specimens have become available since Holdich’s studies, which make the clarification and updating of distribution maps along the NE Atlantic-Black Sea axis necessary. This is particularly so because many of the records for the Mediterranean and Adriatic relate to D. torelliae, which has been synonymized with D. bicolor.

In order to be able to identify species of Dynamene, and distinguish them from some other sphaeromatid isopods, it is important to understand how the morphology changes during the life history. Adult males (stage 8) of the various Dynamene species can be distinguished from those of other sphaeromatid isopods, e.g., Campecopea Leach, 1814; Cymodoce Leach, 1814; Ischyromene Racovitza, 1908; Lekanosphaera Verhoeff, 1943 and Sphaeroma Bosc, 1802, that may be found in the same habitat, by a large two-pronged medial process (the bidentate process) arising from the dorsal posterior margin of the sixth pereonite (Fig. 1). This characteristic is unique to the genus (Harrison and Ellis 1991). Some species of Oxinasphaera Bruce, 1997 have such a process, but this arises from the pleon (Bruce 1997, Schotte and Kensley 2005), and paired processes arise from the seventh pereonite in Dynamenella dioxus Barnard, 1914. Juveniles and females, and even sub-adult males (stages 6 and 7), are more difficult to distinguish between the species, and may also be confused with females of other genera. Vieira et al. (2015) have shown clear differences between D. bidentata, D. magnitorata and D. edwardsi at the genetic level using cytochrome oxidase I (COI-5P). Details of the changes occurring throughout the life history of the best-studied species, D. bidentata, are given below.

Figure 1.

Adult male (stage 8) and pre-ovigerous female (stage 7) Dynamene bidentata. A Dorsal view of stage 7 female B Lateral view of pleon (with posterior border of pereonite 7), pleotelson and right uropod of stage 7 female C Ventral view of pleotelson and uropods of stage 7 female D Dorsal view of stage 8 male E Lateral view of pereonal segment 6, pleon, and pleotelson and exopod of right uropod of stage 8 male. Adapted from Holdich (1968b).

Dynamene species are present in a wide-range of habitats, but usually amongst algae and in cryptic habitats, e.g., under rocks, crevices, empty barnacle tests, amongst serpulid and tunicate colonies, mussel beds and encrusting sponges, from midlittoral to shallow sublittoral levels (Holdich 1970, 1976). Dynamene bidentata, at least, has a biphasic life cycle with a change of habitat, where the immature stages are present amongst the algal cover (which they eat), whilst the adults occupy cryptic habitats where they reproduce and where females can incubate their broods in relative safety (Holdich 1968b, 1970, 1976). Further details of the habitats occupied by Dynamene along the NE Atlantic-Black Sea axis are given for each species below.

Given that fully adult males may not be present in many collections, species identification is often difficult and leads to incorrect assignments, questioning the validity of the information about the actual distribution of the species. The literature is scattered with misidentifications, which have come to light when such authors’ material and/or publications have been examined by us. In the present study we aim to update and correct the geographical distribution of the six described species of Dynamene from the NE Atlantic-Black Sea axis. To facilitate identification, keys to adult males and females of these six species are provided along with associated photographs. It is hoped that these will enable those involved in littoral and sublittoral surveys in the marine environment to identify species of Dynamene more easily.

Methods

The records of David Holdich (DMH) used in this study are derived from field work carried out in various localities in the British Isles, Atlantic islands, Atlantic coasts of mainland Europe, and the Mediterranean and Aegean Seas (Holdich 1968a, c, 1970, Holdich and Lincoln 1974, Holdich 1976). In addition, there have been donations from many colleagues between 1970 and 2014 (see Acknowledgments). Other samples deposited in several museum collections, particularly those in Leiden, Lisbon, London and Paris (see Acknowledgements), and dating back to the 1920s, have been examined. Also, the Dynamene specimens (deposited at the Universities of Aveiro and Minho) collected by Pedro Vieira, Henrique Queiroga and Filipe Costa with the help of other colleagues (see Acknowledgments) were used to supplement the collections. These samples were collected from the NE Atlantic coasts and the Macaronesian archipelagos of Madeira, Azores and Canary islands, between 2009 and 2015. Samples were taken from rocky shore habitats by scraping of the algal cover and hand picking during low tide.

All specimens of Dynamene from DMH’s collections have been deposited in the Naturalis Biodiversity Centre, Leiden, The Netherlands under the catalogue numbers: RMNH.CRUS.1. 7517-7616 and 7642-7676. Specimens of Dynamene already present in the Leiden collections have the catalogue numbers: RMNH.CRUS.1. 7450-7514.

In most cases the only records considered were of specimens actually seen by the authors, confirmed by molecular tools (unpublished data), or where there were clear diagrams in the literature. Although Holdich (1968c) confirmed many specimens from England and Wales during his surveys, since that time most records of D. bidentata have mainly come about as part of the general fauna collected in marine surveys. So, although many records exist in various British databases, particularly those held in the National Biodiversity Network Gateway and ERICA (see Acknowledgements), the current authors have not tried to track down voucher specimens, but have relied on identifications being correct as only one species of Dynamene is indigenous to the British Isles, thus making records more reliable. Details of all the specimens examined in the current study are given in Suppl. material 1.

Using information in the databases, maps were constructed of the six Dynamene species occurring along the NE Atlantic-Black Sea axis using the software ARCGIS 10.3.

Keys and photographic montages based on the main characters of adult males (stage 8) and females are given at the end of the paper. To construct the montages, photographs of alcohol preserved specimens were taken with a Dino-Eye Microscope Camera attached to a Wild M5 binocular microscope via a phototube. Images were edited using appropriate software on a computer.

Results

In this section a generic description of Dynamene is given, followed by details of each of the six species present along the North East Atlantic-Black Sea axis. Keys to and photographs of males and females of each species are given at the end of the paper. Comparisons are made in the main discussion section and overall conclusions are dealt with in the final section. Details of the material examined and geographical coordinates of locations are given in Suppl. materials 1 and 2.

Dynamene Leach, 1814

Synonymy

Nesaea: Leach (1814).

Prochonaesea: Hesse (1873).

Sorrentosphaera: Verhoeff (1944).

Diagnosis

Eubranchiate sphaeromatid with body approximately elliptical. Anteriorly, cephalosome separating the bases of the antennules. Eyes set slightly into pereonal tergite 1. Coxal plates of pereonites 1–7 separated from tergites by sutures.The seventh somite is overlapped by the sixth in adult males (stage 8), with the pleura extended postero-laterally into two small processes, which vary in shape according to species. Pleotelson domed or keeled, and terminating in an obvious terminal foramen, which may be enclosed forming a tube. Antennular peduncle articles 1 and 2 dilated and juxtaposed to ventral margins of cephalosome. All pereopods ambulatory. Both rami of pleopods 1-3 bearing margin of plumose setae. Endopods of uropod fused with protopods and juxtaposed to pleotelsonic margin; exopods posteriorly directed. Sexual dimorphism pronounced. Adult male with pereonal tergite 6 longer than those preceding, posterior margin with an elongate, posteriorly directed process either side of the mid-line (the bidentate process). Posterior part of pleotelson with central boss. Penes small, separate. Endopod of pleopod 2 lacking appendix masculina. Female with pereonal tergite 7 similar to those preceding and lacking bidentate process; pleotelson smooth. Ovigerous female with ventral marsupium, formed from four pairs of lamellae, which arise from pereonites 1-4. Mouthparts strongly metamorphosed.

Type species

Oniscus bidentatus Adams, 1800

Dynamene bidentata (Adams, 1800)

Restricted synonymy

Oniscus bidentatus: Adams (1800).

Naesa bidentata: Leach (1815).

Dynamene bidentata: Holdich (1968a, b, c, 1969, 1970, 1971, 1976); Kussakin (1979); Harrison and Ellis (1991).

An extensive synonymy was given by Holdich (1968a, c) for citations prior to 1968.

Material examined

Specimens have been examined from 129 locations in the NE Atlantic, mainly from the British Isles, Channel Islands, France, Spain, Portugal and Morocco – see the Suppl. materials 1 and 2. A number of literature records have been included where the diagrams clearly indicate this species. In addition, there are 76 records from the NBN database.

Key morphological characters

Body convex; in stage 8 males the pleotelsonic boss is large and bilobed, the two halves are separated by a wide v-shaped groove; the arms of the bidentate process taper to a point, and are sparsely rugose dorsally (Fig. 2A–B). In stage 7 females the pleotelsonic dome is smoothly rounded in side view and the pleotelsonic foramen is open and flush with the edge of the pleotelson (Fig. 3A–B). In populations from Atlantic coasts the smooth outline of the pleotelsonic dome in females and juveniles is key to separating this species from D. magnitorata and D. edwardsi, where it is keeled in side view. Further details are provided by the scanning electron microscope pictures of the posterior body of a stage 8 male and a stage 7 female in Holdich (1976).

Figure 2.

Main features of adult males (stage 8) of the NE Atlantic-Black Sea axis Dynamene spp. A, B D. bidentata (S. Wales). Arrows indicate shape of the bidentate process (A), uropods (A, B) and pleotelsonic boss (B) C, D D. magnitorata (Roscoff, France). Arrows indicate shape of the bidentate process (C), the uropods (C, D) and the pleotelsonic boss (C, D). Note the difference in the shape of the boss and the ends of the arms of the bidentate process to those of D. bidentata E, F D. edwardsi (E Canaries F Azores). Arrows indicate shape of the bidentate process (E, F), uropods (F) and pleotelsonic boss (E, F). Specimen in E shows relatively little dorso-lateral setation, whilst that in F is hirsute. Note the differences in the shape of the boss and the tips of the arms of the bidentate process compared to those of D. bidentata and D. magnitorata G, H D. bifida (France, Mediterranean). Arrows indicate shape of the bidentate process (G, H), uropodal exopod (H) and pleotelsonic boss (G). Note the large accessory process on each arm of the bidentate process, the small sessile pleotelsonic boss and the long narrow uropodal exopods I D. tubicauda (Bay of Naples, Italy). Arrows indicate the unique body shape, tubular respiratory channel, peg-like pleotelsonic bosses, and the curved uropodal exopods J, K D. bicolor (Bay of Naples, Italy). Arrows indicate shape of the bidentate process (J), and pleotelsonic boss (J, K). Note in particular the rugose nature of the dorsal surface of the bidentate arms, and the triangular shape of each half of the boss – in specimens from the Black Sea the boss is of a similar shape but much less prominent.

Figure 3.

Main features of females and juveniles of the NE Atlantic-Black Sea axis Dynamene spp. A, B Dynamene bidentata (S. Wales). Arrows indicate smooth outline of pleotelsonic dome (A) and non-tubular pleotelsonic foramen (B) C, D Dynamene magnitorata (Roscoff, France). Arrows indicate angular outline of pleotelsonic dome (C), posterior extension of pleotelsonic keel and non-tubular pleotelsonic foramen (D) E, F, G Dynamene edwardsi (Italy). Arrows indicate angular outline of pleotelsonic dome (E) with central bulge (E, F, G) and tubular pleotelsonic foramen. (E and F from Naples, Italy G hirsute female from the Venice Lagoon, Italy) H, I Dynamene bicolor (Naples, Italy). Arrows indicate angular outline of pleotelsonic dome (I) and non-tubular pleotelsonic foramen (H) J, K Dynamene tubicauda (Ischia, Italy). Arrows indicate flattened epimera surrounding body that give this species a unique body shape (J, K) and the tubular pleotelsonic foramen (J, K) L, M. Dynamene bifida (Ischia, Italy). Arrows indicate smooth outline to pleotelsonic dome (L) and pleotelsonic foramen at end of short tube (M).

Size

Adult males (stage 8) typically 7.0 × 3.0 mm, although specimens 10 mm in length have been seen; pre-ovigerous females (stage 7) typically 6.0 × 2.9 mm.

Life-history

There are eight life-history stages in both males and females (Holdich 1968b). Sexual dimorphism becomes apparent in stage 6 males with the appearance of a very small bidentate process, this increases in size at the seventh, and is fully developed by the eighth and terminal stage (Figs 1D, 4–lower row 6–8). This process is absent from juveniles and females (Figs 1A-B, 4–upper row 6–8, 2A–M). Juveniles and females up to and including stage 7 are very similar to each other morphologically. At the moult to stage 8 females become ovigerous and are very similar morphologically between the species. Their mouthparts are strongly metamorphosed, and they die after releasing their broods (Hansen 1905, Holdich 1968b, 1971). Stage 8 males live for two breeding seasons, at least in the British Isles, and remain in their cryptic habitat for the entire period without apparently feeding (Holdich 1971). Those in their second year are recognizable from the growths of algae, and sometimes serpulids, on the pleotelson.

Figure 4.

Dorsal views of the posterior halves of the bodies of various life history stages (5–8) of Dynamene bidentata. 5 juvenile Upper row female stages 6, 7, 8 (ovigerous) Lower row male stages 6, 7, 8. Adapted from Holdich 1968b.

Habitat

All stages can be found on a wide variety of mid- to lower littoral algae, and also in rock pools in the upper littoral zone. Fenwick (pers. comm., July 2016) has found this species commonly amongst lower shore and sublittoral coralline algae in Cornwall, and he has also recorded adults from under large lower shore pebbles. Stage 7 females and stage 8 males move from the algae into cryptic habitats, such as crevices and empty barnacle tests, particularly Balanus perforatus, to breed (Holdich 1970, 1976). Stage 7 females moult into stage 8 females within such a habitat and reach peak numbers in April/May each year (Holdich 1968b).

Colour

Some degree of camouflage in the algal habitat is given by green, yellow and brown ‘uniformis’ phenotypic varieties, and this is enhanced by the development in some individuals of patterns of white or red, dorsal, non-adaptable chromatophores (Tinturier-Hamelin 1962, 1967, Holdich 1969, Arrontes 2009). In the past some workers have given specific status to the red and green colour varieties, e.g. rubra and viridis (see Holdich 1968c). Adult males are particularly colourful when found amongst red algae on the lower shore, with the margins of the body segments and uropods bordered in orange.

Geographical distribution

The distribution of this species shown in Holdich (1970, 1974) has been extended by the present study. It occurs from the Shetland Islands to Tarfaya in western Morocco and Tenerife and Gran Canaria in the Canary Islands, which are the only two records of the species in Macaronesia (Fig. 5A). Within this range D. bidentata occurs in the north, northwest (including the outer islands), west and south coasts (as far as the Isle of Wight) of Great Britain, around Northern and Southern Ireland, the Channel Islands, northwest France, Atlantic Iberian Peninsula and in northwest Africa. Arrontes (1991) cites D. bidentata as being the most abundant isopod species on shores in northern Spain. It is the only species present in the British Isles (with the exception of a single record of D. magnitorata in southern England). It is particularly common in SW England and SW Wales, especially where the large barnacle, Balanus perforatus is present. There is one recent record for north-eastern England, which may be the result of a stranding, as are records for The Netherlands, where it is not considered indigenous (Holthuis 1956). The closest record to the Mediterranean of D. bidentata is Tarifa, in southern Spain (Guerra-García et al. 2011, Izquierdo and Guerra-García 2011, Guerra-García et al. 2012, Torrecilla-Roca and Guerra-García 2012).

Figure 5.

Distribution of Dynamene species along the NE Atlantic-Black Sea axis based on material validated during the present study. A Dynamene bidentata B Dynamene bicolor C Dynamene bifida D Dynamene edwardsi E Dynamene magnitorata F Dynamene tubicauda.

Remarks

Maggiore and Fresi (1984) described D. bidentata from the Gulf of Naples (publishing descriptions and figures), and several authors (e.g., Castelló and Carballo 2001, Castellanos et al. 2003, Junoy and Castelló 2003) have used Maggiore and Fresi’s (1984) observations to justify their findings of D. bidentata in the Mediterranean. Yet, examination of the single specimen found by Maggiore and Fresi (1984) showed that it was in fact a D. magnitorata.

A lot of confusion regarding the identification of D. bidentata was caused by Torelli (1930) who figured what she called D. bidentata (a stage 8 male and a stage 8 ovigerous female), from the Bay of Naples, Italy. Omer-Cooper and Rawson (1934) used Torelli’s figures to illustrate D. bidentata from Britain, which was then proliferated in some British identification guides, e.g., Barrett and Yonge (1964), although this has been corrected in more modern guides, e.g., Hayward and Ryland (1995). Pauli (1954) also used Torelli’s figures to illustrate D. bidentata from the Black Sea. Holdich (1968a) collected material from Naples and decided that Torelli’s figures were in fact of a new species, commonly found in the Bay of Naples, which he named D. torelliae Holdich, 1968. However, Kussakin (1979) decided that D. torelliae was in fact synonymous with D. bicolor (Rathke, 1837). This species was in fact unknown to Holdich at the time of his studies.

Databases we have consulted indicate that D. bidentata commonly occurs around Northern and Southern Ireland. However, we could only find one modern published record, i.e., de Grave and Holmes (1998) from Lough Hyne in County Cork.

Unlike most other isopods, stage 8 male Dynamene bidentata do not have appendix masculina on the endopods of the second pair of pleopods, this is also the case in the other Dynamene species. This phenomenon has also been noted by Messana (2004) in Sphaeroma terebrans Bate, 1866. It is very difficult to observe mating in Dynamene due to the cryptic habitat of the adults. It is probable that sperm are released directly into the marsupium as the eggs are laid.

Dynamene bicolor (Rathke, 1837)

Restricted synonymy

Campecopea bicolor: Rathke (1837).

Dynamene bidentata: Torelli (1930); Omer-Cooper and Rawson (1934); Pauli (1954); Holthuis (1956); Barrett and Yonge (1964); [not D. bidentata of Adams (1800)].

Dynamene torelliae: Holdich (1968, 1970).

Dynamene bicolor: Kussakin (1979); Maggiore and Fresi (1984).

Material examined

Specimens have been examined from 48 locations in 12 countries in the Mediterranean and Black Seas - see the Suppl. materials 1 and 2. A number of literature records have been included where the diagrams clearly indicate this species.

Key morphological characters

In stage 8 males the pleotelsonic boss is comprised of two right-angled triangular structures separated by a deep groove (however, the boss may be very low lying in some specimens, e.g., those from the Black Sea); the arms of bidentate process taper to a point and are rugose dorsally (Fig. 2J–K). In stage 7 females the pleotelsonic dome is keeled in side view and the pleotelsonic foramen is flush with the edge of the pleotelson (Fig. 3H, I). The females of this species are very difficult to separate from those of D. magnitorata. Maggiore and Fresi (1984) provide a complete description of D. bicolor.

Size

Adult males (stage 8) typically 3.5 × 1.5 mm, pre-ovigerous females (stage 7) typically 3.0 × 1.3 mm.

Life-history

Nothing is known of the life-history, other than the fact that sexual dimorphism occurs with males developing the bidentate process characteristic of the genus.

Habitat

Juveniles are usually found in shallow water on a variety of algae down to 3.0 m and adults in empty Balanus tests, in mussel beds, in rock crevices, within sponges, and under rocks throughout the Mediterranean. However, occasionally they have been found in deeper water, e.g., off the island of Chios (Greece) specimens were collected from Cystoseira at depths from 0.5 – 30 m (see Suppl. material 1).

Colour

As with D. bidentata, some degree of camouflage in the algal habitat is given by yellow or dull green ‘uniformis’ phenotypic varieties, and this is enhanced by the development in some individuals of patterns of white or red, dorsal, non-adaptable chromatophores (Holdich 1969).

Geographical distribution

The distribution of this species shown in Holdich (1970) has been extended by the present study. It is the most commonly recorded Dynamene species in the Mediterranean, occurring from the Balearic Islands in the west to the coast of Israel in the east, although there are only a few records for the North African coast (Fig. 5B). It has been frequently recorded around the Greek islands and mainland coast of both Greece and Turkey. The most northerly record is for Croatia in the Aegean Sea. It has also been recorded for a number of countries around the Black Sea (Bulgaria, Romania, Turkey and Georgia) (Fig. 5B). Most records in the literature refer to D. torelliae, which is now considered synonymous with D. bicolor.

Remarks

Many records exist, both published and unpublished, for Dynamene bicolor (usually as ‘D. torelliae’) in the Mediterranean Sea, particularly from the coasts of Spain, France, Italy and Greece (Holdich 1970, Bakir et al. 2014). However, its presence in Egypt and Israel was unreported until now. Previous observations indicated its presence in the Black Sea (Kussakin 1979), where it was thought to be the only Dynamene species present (Gönlügür-Demirci and Katağan 2004). On comparing specimens from the Black and Mediterranean Seas the current authors have accepted the decision of Kussakin (1979) that D. torelliae and D. bicolor are synonymous. However, it is clear that some of the specimens from the Black Sea have a reduced pleotelsonic boss, and the two may eventually turn out to be separate species when more material is examined. Kirkim et al. (2006) commented on the form of the pleotelsonic boss, stating that this can vary from two small projections to a well-formed boss in specimens of ‘D. torelliae’ from the Aegean Sea. Rathke’s (1837) drawings of D. bicolor show the posterior halves of a female and a stage 7 male. The male has two joined hemispherical pleotelsonic bosses, which are similar to those found in the same stage of ‘D. torelliae’ and unlike that of D. edwardsi the other species in the region, which is single.

Dynamene bifida Torelli, 1930

Restricted synonymy

Dynamene bifida: Torelli (1930).

Dynamene bifida: Holdich (1968, 1970).

Material examined

Specimens were examined from seven locations in Spain, Greece, France, Italy and Turkey in the Mediterranean – see the Suppl. materials 1 and 2. A number of literature records have been included where the diagrams clearly indicate this species.

Key morphological characters

In stage 8 males each arm of the bidentate process is large, tapering and with a well-developed, downwardly-directed accessory process a quarter of the way from the apex; the pleotelsonic boss is very small with raised pointed corners (Fig. 2G–H). In stage 7 females the pleotelsonic dome is smoothly rounded in side view and the pleotelsonic foramen is at the end of short tube (Fig. 3L–M).

Size

Adult males (stage 8) typically 5.0 × 3.0 mm, although a specimen of 7.0 mm length has been seen; pre-ovigerous females (stage 7) typically 4.0 × 2.0 mm.

Life-history

Nothing is known of the life-history of this species, other than the fact that sexual dimorphism occurs with males developing the bidentate process characteristic of the genus.

Habitat

Adults, including stage 8 females, were found among Hydroides unicata colonies and other cryptic habitats in the Bay of Naples (Torelli 1930, Holdich 1970). Ledoyer (1962) recorded it from Ulva lactuca at Endoume, southern France, and Holthuis (unpublished records) from rocky shores amongst algae at 0.0–1.0 m at Banyuls-sur-Mer. The latter record included stage 8 females.

Colour

All specimens seen were a pale, sandy yellow. No polychromatism was observed.

Geographical distribution

The distribution of this species shown in Holdich (1970) has been extended by the present study. It has a widespread distribution in the Mediterranean stretching from southern Spain to Turkey (Fig. 5C).

Remarks

Originally described by Torelli (1930) from the Bay of Naples, males of this distinctive, and sometimes large, species has been infrequently recorded, and females even less so. The accessory process on each arm of the bidentate process is similar to that found in the Australian species, D. ramuscula (Holdich and Harrison 1980). The fact that ovigerous females were found amongst shallow-water algae raises questions about the life-history of this species, although in the Bay of Naples this stage has been recorded with males in more protective habitats.

Dynamene edwardsi (Lucas, 1849)

Restricted synonymy

Naesa edwardsi: Lucas (1849).

Dynamene hanseni: Monod (1923).

Dynamene edwardsi: Holdich (1968a, 1970); Harrison (1982).

Dynamene bidentata: Picker and Griffiths (2011).

An extensive synonymy was given by Holdich (1968a, c) for citations prior to 1968.

Material examined

Specimens were examined from 89 locations in NE Atlantic, Mediterranean, Adriatic, Aegean and Red Seas – see Suppl. materials 1 and 2. A number of literature records, e.g., the Suez Canal, have been included where the diagrams clearly indicate this species.

Life-history

Nothing is known of the life-history of this species, other than the fact that sexual dimorphism occurs with males developing the bidentate process characteristic of the genus.

Key morphological characters

Body convex; in stage 8 males the apices of arms of the bidentate process are swollen, each with a short, downwardly-directed spur; the pleotelsonic boss is plate-like with two forward-facing pegs; the body exhibits various degree of setation (Fig. 2E–F), e.g., specimens examined from the Balearic Islands (Spain) and the island of Chios (Greece) are somewhat different from other D. edwardsi seen by us in being very hirsute, with a pronounced developing boss and respiratory tube in the stage 7 males. In stage 7 females the pleotelsonic dome is keeled in side view, with a median protuberance; the pleotelsonic foramen is at the end of a short tube (Fig. 3E–G). Further details are provided by the scanning electron microscope pictures of the posterior body of a stage 8 male and a stage 7 female in Holdich (1976). See keys to stage 8 males and stage 7 females.

Size

Adult males (Stage 8) typically 5.5 × 2.25 mm; pre-ovigerous females (stage 7) typically 3.0 × 1.1 mm, specimens of 4.4 × 2.3 mm have been seen from the Venice Lagoon, Italy.

Habitat

Juveniles and adults have been found amongst a variety brown, green and red algae in the littoral and sublittoral zones, sometimes in conjunction with D. bicolor in the Mediterranean, and with D. bidentata and D. magnitorata on Atlantic coasts. Adults have also been recorded from amongst mussels and tube worm colonies and barnacle tests in the Bay of Naples (Torelli 1930, Holdich 1970), and elsewhere in the Mediterranean (e.g., Rivosecchi 1961, Bellan-Santini 1962). It has been found associated with encrusting matter on solid surfaces in some harbours and canals. On occasions it has been found amongst the ‘trottoir’ on steep-sided cliffs as deep as 10 m. Monod (1932) recorded it from coralline and fucoid algae on the coast of NW Africa. In the Azores, adults have been recorded from empty Chthamalus stellatus tests attached to lower shore cobbles, along with Campecopea lusitanica. In West Portugal (Buarcos) it is present with D. bidentata and D. magnitorata. However, while D. bidentata adults were present in barnacles, no D. edwardsi were found inside barnacles, only among intertidal algae and on a few ‘small’ algae in shaded crevices at 0-1 m. Also, they were not present among mussels. Unusually, adults, including stage 8 females, were found in upper shore sandstone crevices, along with Campecopea hirsuta, in southern Portugal.

Colour

The general body colour is a dull grey-green, individuals sometimes exhibit polychromatism caused by patterns of white, dorsal, non-adaptable chromatophores as seen in some of the other species (Holdich 1969).

Geographical distribution

The distribution of this species shown in Holdich (1970) has been extended by the present study. It is the most meridional of the Atlantic species, occurring from Galicia in north-western Spain to Nouadhibou in Mauritania (Fig. 5D). This is the currently known southern limit of Dynamene species of the NE Atlantic-Black Sea axis. It is widespread in the Macaronesian islands and in the eastern and western Mediterranean (Fig. 5D). The most northerly record comes from the Venice Lagoon in the Adriatic Sea. It is also the only Dynamene species recorded from the Red Sea, in the Gulf of Aqaba (Fig. 5D). Glynn (1972) recorded a species that is clearly D. edwardsi from the Suez Canal. Picker and Griffiths (2011) have recorded this species (as D. bidentata) from South Africa.

Remarks

Dynamene edwardsi occupies a wide vertical range in the littoral zone on NE Atlantic shores, and from the littoral zone down to 10 m in the Mediterranean. In recent field work, it was found to be very abundant in the Canary Islands and Madeira archipelago, whereas D. magnitorata was more common in the Azores and D. edwardsi rare. It is the most southerly of the Dynamene species extending down the West African coast to Mauritania and the only record for tropical waters. Glynn (1972) suggested that D. edwardsi has migrated from the Mediterranean throughout the whole length of the canal. Our study has shown that it has now reached the Gulf of Aqaba in the Red Sea

The records for the Suez Canal and Red Sea are interesting as they show movement from the Mediterranean Sea into the Red Sea, whilst many marine species are moving in the opposite direction (Galil et al. 2014). No Dynamene species have yet been recorded from the Indian Ocean (Schotte and Kensley 2005). However, a stage 8 male has been recorded from Port Elizabeth harbour in South Africa by Picker and Griffiths (2011). They suggest that it may have been introduced as a fouling organism or in ballast water. It is known that this species can be transported amongst fouling organisms on ships, as evidenced by the finding a stage 8 male on a ship in Tangiers harbour (Morocco) (see Suppl. material 1).

This species is variable in its morphology and particularly in the degree of hirsuteness. It may be that some of the specimens collected from the Balearic and Greek islands are in fact a new species, but more material is needed to prove this. Ideally, a molecular genetic analysis needs to be carried out on Mediterranean and Adriatic specimens. Such a technique applied to specimens from some NE Atlantic coasts and Macaronesian islands has shown that a number of cryptic species may be present (Vieira et al. 2015).

Dynamene magnitorata Holdich, 1968

Restricted synonymy

Dynamene magnitorata: Holdich (1968).

Dynamene bidentata: Monod (1932); Maggiore and Fresi (1984).

Dynamene magnitorata: Holdich (1968a, 1970, 1976).

Material examined

Specimens were examined from 52 locations in the NE Atlantic, and four countries in the Mediterranean – see the Suppl. materials 1 and 2. A number of literature records have been included where the diagrams clearly indicate this species.

Key morphological characters

Body convex; in stage 8 males the pleotelsonic boss is large, bilobed, with the two halves separated by a narrow groove; the arms of the bidentate process are of similar width along their lengths and are dorsally tuberculate (Holdich 1976, fig. 3A, B; Fig. 2C–D in this paper). In stage 7 females the pleotelsonic dome is keeled in side view and the pleotelsonic foramen is flush with the edge of the pleotelson (Fig. 3C–D). Further details are provided by the scanning electron microscope pictures of the posterior body of a stage 8 male and a stage 7 female in Holdich (1976). The females of this species are very difficult to separate from those of D. bicolor. See keys to stage 8 males and stage 7 females.

Size

Adult males (stage 8) typically 4.25 × 2.25 mm, pre-ovigerous females (stage 7) typically 4.0 × 2.0 mm.

Life-history

A comparison of the life-histories of D. bidentata and D. magnitorata from two Atlantic coast locations was made by Holdich (1976). Only a limited number of D. magnitorata specimens were available but it showed that this species has a similar sequence of seasonal events (see description for D. bidentata). However, whereas D. bidentata stage 8 males live for two breeding seasons, those of D. magnitorata may only live for one.

Habitat

A mid- to lower littoral and shallow sublittoral species, although sometimes recorded from deeper water. Its range occasionally overlaps that of D. bidentata. Juveniles are found associated with a wide range of littoral and shallow water algae, particularly Corallina sp., Rhodomenia palmata, Chondrus cripspus and Gigartina stellata. Adults have been found in empty tests of Balanus crenatus, amongst ascidians, and in channels within sponges (including those associated with eel grass beds). In the Roscoff region (northern France) adults were frequently found within the encrusting sponge, Halichondria sp. In the Azores (São Miguel island) adults have been found sublittorally in the empty tests of Megabalanus azoricus, as well as intertidally among algae on the islands of Terceira, São Miguel and Santa Maria. On Fuerteventura (Canary Islands) adult males were caught using a surface dip net. In the Chafarinas Islands off Mediterranean Morocco they have been recorded from 0.0m down to 20.0 m on a variety of algae. Like Dynamene bidentata (Harvey et al. 1973), D. magnitorata adults were found to have a tolerance to high air temperatures, i.e., 38 °C (Holdich 1976). However, survival at 5 °C was much lower for D. magnitorata compared to D. bidentata (Holdich 1976) and this may be the reason it has not colonized more northerly regions.

Colour

Individuals exhibit a wide variety of colours, often matching the colour of their background, the predominant colours being coralline-pink and brown, rather than the greens and yellows seen in D. bidentata. Individuals sometimes exhibit polychromatism caused by white, dorsal, non-adaptable chromatophores, as seen some other species (Holdich 1969, 1976).

Geographical distribution

The distribution of this species shown in Holdich (1970) has been extended by the present study. It has been recorded from southern England (a single specimen only that may be the result of a stranding), the Channel Islands, around the coasts of Brittany, the Atlantic Iberian Peninsula and northwest Africa, the islands of the Azores, Canary Islands and Madeira in the Macaronesian archipelagos, and in the Mediterranean along the European and African coasts, and also Egypt (Fig. 5E).

Remarks

Almost all the Dynamene specimens found in the Azores during recent field work belonged to D. magnitorata. However, Dynamene was less prevalent in the benthic community when comparing with Canaries and Portugal (pers. obs., unpublished data). Maggiore and Fresi (1984) described D. bidentata from the Bay of Naples, but in fact examination of the specimen showed it to be a male D. magnitorata. If the author’s had compared an actual D. bidentata with their specimen then they would have realized this, particular as it is so much smaller than any known D. bidentata specimen. Dynamene magnitorata has only rarely been recorded in the Mediterranean, i.e. twice in Spain, and once in each of Egypt, Italy, Monaco and Tunisia, although it was found to be common on the Chafarinas Islands off Morocco (Castellanos et al. 2003) (see Suppl. material 1).

Dynamene tubicauda Holdich, 1968

Restricted synonymy

Dynamene tubicauda Holdich (1968).

Dynamene tubicauda: Holdich (1968a, 1970); Lombardo (1984); Borg et al. (2006).

Material examined

Specimens were examined from six Italian locations in the Bay of Naples and off the island of Elba, and one location off Malta - see the Suppl. materials 1 and 2. A number of literature records from Sicily have been included as the diagrams clearly indicate this species (Lombardo 1984).

Key morphological characters

The morphology of this species is unique amongst the known Dynamene species - in stage 8 males the pereon length and width are similar; the epimera and front of the head form a shelf; the antennular peduncle is expanded; there are two widely separated, peg-like pleotelsonic bosses; and the pleotelsonic foramen is at the end of a ventrally-closed tube (Fig. 2I). In stage 7 females the body is also flattened with the epimera forming a shelf round the body; the pleotelsonic foramen is at the end of a well-developed tube (Figs 3J–K). See keys to stage 8 males and stage 7 females.

Size

Adult males (stage 8) typically 3.0 × 2.0 mm, pre-ovigerous females (stage 7) typically 2.5 × 2.0 mm.

Life-history

Nothing is known of the life-history of this species, other than the fact that sexual dimorphism occurs with males developing the bidentate process characteristic of the genus. Holdich (1968) only recorded males, but both sexes have been recorded in the present study. Lombardo (1984) was the first to describe the adult female.

Habitat

This species has been found between 2-30 m amongst algae in muddy/sandy and coralline habitats, rock scrapings, freely swimming at 30 m, and also in sea grass meadows (Lombardo 1984, Borg et al. 2006).

Colour

Pale yellow. No polychromatism was observed.

Geographical distribution

The distribution of this species shown in Holdich (1970) has been extended by the present study. However, it appears to be restricted to the eastern Mediterranean, having only been recorded off the west coast of Italy (Holdich 1968), Sicily (Lombardo 1984) and Malta (Borg et al. 2006) (Fig. 5F). The most northerly record is for the island of Elba and the most southerly is off Malta.

Remarks

The distribution of this species is the most restricted of all the Dynamene species along the NE Atlantic-Black Sea axis. Considering the large number of samples examined during this study this restricted distribution is most likely real. Its unusual flattened shape and the position of the pleotelsonic foramen at the end of a tube, even in adult males, may be an adaptation to inhabiting sediments.

Dynamene sp.

Material examined

Two stage 8 males. See the Suppl. materials 1 and 2.

Key morphological characters

The bilobed pleotelsonic boss has a posteriorly-directed spine not seen in any other stage 8 males. The uropodal exopod is wide and the body markedly hirsute.

Habitat

Known only from the stomach contents of a black scorpionfish Scorpaena porcus.

Geographical distribution

Known only known from NW Aegean Sea.

Remarks

Only two specimens have been found, both stage 8 males, and both from the stomach contents of a black scorpionfish, Scorpaena porcus. This could well be a new species of Dynamene, but more material is needed to confirm this. It may even be related to the hirsute specimens found in the Balearic Islands and the Greek island of Chios. The fish is known to be a bottom feeder in the Black Sea, close to where the specimen came from, which was in the NW Aegean, where it occurs at 20–40 m depth (Başçïnar and Saǧlam 2009). Rafrafi-Nouira et al. (2016) examined the diet of S. porcus from waters off the coast of Tunisia, but the only isopods they found were listed as unidentified.

Discussion

Three species of Dynamene occur on the shores of the continent and islands of the NE Atlantic Ocean (D. bidentata, D. magnitorata and D. edwardsi). In recent field work, no Dynamene specimens were collected in Scandinavia or Iceland (pers. obs., unpublished data). This is probably due to the fact that members of this genus may not be able to tolerate cold water and weather. For example, studies by Holdich (1968b, c, 1970) were meant to be carried out on the Gower Peninsula in South Wales, but the severe and long-lasting winter of 1962-1963 decimated the populations, as well as those of Balanus perforatus, and the study site was relocated to western Pembrokshire in 1964 (SW Wales), where the populations of both were unaffected. Moyse and Nelson-Smith (1964) showed that when sea and air temperatures were below 5 °C for a long period, viable broods were not produced by females of D. bidentata. Moreover, with lower average air temperatures, populations of Dynamene must restrict their growth phases to fewer months of the year (Holdich 1976). The previously known northerly limit of Dynamene was Ardrossan in the west of Scotland (Holdich 1970). In this study, we extended the northern range of this genus to Clatholl in the north of Scotland, and recent surveys by British workers have shown that it also occurs in the Shetland Islands north of Scotland. There are a number of records for the Western Isles off Scotland (Fig. 5A) that are warmed by the Gulf Stream. However, one record is shown from north-eastern England (Fig. 5A), which tends to be colder than the west coast due to a lack of influence from the Gulf Stream, but it is not known if a permanent population exists there. It may represent a stranding from a population elsewhere. Holthuis (1956) recorded D. bidentata from the other side of the North Sea in The Netherlands. He was of the opinion that it was not indigenous there, but was occasionally stranded with flotsam and jetsam. There are old records in the literature of D. bidentata for eastern Scotland (Scott 1899) and also for south-east England (Butler 1878), but none (other than the record mentioned above) have come to light in the last few decades.

Dynamene bidentata is the only species present in the British Isles (Holdich 1969, 1970; Holdich and Lincoln 1974). Although in our databases there is a record of Dynamene magnitorata in southern England, we believe this probably does not represent an actual permanently established population. However, D. magnitorata is common on Guernsey (Channel Islands), which is not that far geographically from the south of England. According to Holdich (1970), and confirmed by the current study, D. bidentata is distributed along the Atlantic coasts of Europe from the northern British Isles to Portugal. Barrois (1888) recorded D. bidentata from the Azores, and it is listed as being present there by Ferraz et al. (2004) and Borges et al. (2010). Rodrigues (1990) recorded it as being common on the island of Flores. However, none of the specimens we have examined from the Azores have been of this species, and the records may well have been D. magnitorata or D. edwardsi. Pereira et al. (2006), Guerra-García et al. (2011), Izquierdo and Guerra-García (2011), Guerra-García et al. (2012) and Torrecilla-Roca and Guerra-García (2012) recorded it from southern Portugal and southwest Spain, and indicated that these regions as the most meridional locations where this species was collected. Our observations extend the distribution of D. bidentata further south, i.e., Akhfenir in Morocco and Tenerife and Gran Canaria in the Canary Islands. Because D. bidentata can survive at temperatures up to 38 °C (Harvey et al. 1973), it is possible that this species occurs further south.

During the current study the authors examined many collections from the Mediterranean and we did not find any D. bidentata. It has been pointed out above that Torelli’s (1930)D. bidentata’ from the Bay of Naples is in fact D. bicolor, as are a number of other references to D. bidentata in the literature. Also, Maggiore and Fresi’s (1984)D. bidentata’ from the Bay of Naples is a D. magnitorata. From the examination of some other collections we also conclude that Castello’s (1986) ‘D. bidentata’ is an Ischyromene sp., that Kirkim’s (1998)D. bidentata’ is D. bicolor, and that Castellanos’ et al. (2003)D. bidentata’ is D. magnitorata. It is not impossible that D. bidentata occurs in the western Mediterranean as it has been recorded close to the Strait of Gibraltar (Torrecilla-Roca and Guerra-García 2012), but currently there is no evidence for this.

On Atlantic mainland coasts and islands, D. bidentata, D. edwardsi and D. magnitorata are usually present in the midlittoral to sublittoral zones, although occasionally they are found higher up the shore. Usually the juveniles are present among the fronds of brown, red and sometimes green algae, whilst the adults inhabit cryptic habitats such as crevices, empty barnacle tests, mussel beds and encrusting organisms. Individuals often match the colour of the algae they are feeding on and additional camouflage is afforded by linear and globular patterns of white chromatophores on the dorsal surface (Tinturier-Hamelin 1962, Holdich 1969, 1976). In the Mediterranean and Black Seas, D. magnitorata, D. bifida, D. bicolor and D. edwardsi usually inhabit shallow water zones, although the last two species can also be present in deeper water off steep-sided islands. Juveniles of these species inhabit algae whilst adults are usually found in more cryptic habitats, but sometimes amongst algae. Dynamene tubicauda has been found between 2-30 metres amongst algae in muddy/sandy and coralline habitats, rock scrapings, freely swimming at 30 m, and also in sea grass meadows (Lombardo 1984, Borg et al. 2006, Holdich, pers. obs.). The vertical range of D. bicolor is the largest, extending from shallow-water algae and cryptic habitats such as barnacles down to 33 m off steep-sided islands. The vertical ranges of some Dynamene species may overlap, e.g., D. bidentata and D. magnitorata on Atlantic Ocean shores, although the latter usually occurs at a lower level on the shore (Holdich 1970, Arrontes and Anadón 1990a; Castelló and Carballo 2001, Guerra-García et al. 2011, Izquierdo and Guerra-García 2011). Dynamene bicolor and D. edwardsi frequently inhabit the same shallow-water algae in the Mediterranean.

Conclusions

Six species of Dynamene are present along the NE Atlantic-Black Sea axis, and one species extends into the Red Sea. It would appear that D. bidentata is restricted to coastal habitats of the NE Atlantic, no evidence was found to suggest it inhabits the Mediterranean. Dynamene magnitorata has a wider geographical range, occurring on coastal habitats of the NE Atlantic as well as those of the Mediterranean. Dynamene edwardsi has the widest geographical range of the six species under consideration, extending from the Macaronesian archipelagos in the NE Atlantic, down the north-western coast of Africa, through the Mediterranean into the Suez Canal and Red Sea. It is not known if a recent record from South Africa represents an introduction or an established population. Dynamene bicolor, D. bifida and D. tubicauda are restricted to the Mediterranean, although D. bicolor also extends into the Black Sea. Dynamene bicolor is the most commonly found and most wide-spread Dynamene species in the Mediterranean. Dynamene bifida has only been recorded at six locations, but its range extends from southern Spain to Turkey. Dynamene tubicauda has the smallest geographical range having only been recorded for Italy and Malta. Some species have large vertical ranges, having been found intertidally down to 30 m. It is highly probable that some of the records for the Dynamene species are the result of introductions via fouling organisms attached to ocean-going vessels, e.g., D. magnitorata and D. bifida with their sporadic distribution in the Mediterranean, and D. edwardsi in South Africa.

There are still a number of outstanding issues relating to Dynamene that can only be dealt with if more material becomes available. Firstly, the status of the hirsute species from the Balearic Islands and the Greek island of Chios – are these a form of D. edwardsi or a new species? Secondly, the status of ‘D. torelliae’ – is it really synonymous with D. bicolor from the Black Sea? Thirdly, the status of the specimens found in the Scorpaena porcus stomach, which appears different from the other species, but cannot be confirmed until more stage 8 males are found. Fourthly, a genetic analysis of all the species needs to be carried out to ascertain the taxonomic status and species boundaries, and the phylogenetic relationships between species, especially those in the Mediterranean and Black Seas. Currently, only D. bidentata, D. magnitorata and D. edwardsi from NE Atlantic coasts have been analyzed, and have been found to be distinct.

Key to the adult males (stage 8) of Dynamene spp. along the NE Atlantic-Black Sea axis

1 With a bidentate process arising from posterior margin of pereonite 6 - sub-adult and adult ♂ Dynamene (Figs 1, 2, 3) 2
Without bidentate arising from posterior margin of pereonite 6 juvenile and ♀ Dynamene (see key to females)
2 With large bidentate process arising from posterior margin of pereonite 6: adult ♂ Dynamene (Figs 1D, 2A–K) 3
With small or medium bidentate process arising from posterior margin of pereonite 6 sub-adult ♂ Dynamene (Fig. 4–lower row 6-7)
3 Pereon length and width similar; epimera and front of head forming a shelf; antennular peduncle expanded; two widely separated, peg-like pleotelsonic bosses; pleotelsonic foramen at end of a ventrally-closed tube (Fig. 2I) D. tubicauda
Pereon length greater than width, pleura and front of head not forming a shelf; antennular peduncle not expanded; pleotelsonic boss single 4
4 Bidentate processes large, tapering and with a well-developed, downwardly-directed accessory process a quarter of the way from the apex; pleotelsonic boss very small with raised pointed corners (Fig. 2G–H) D. bifida
Bidentate processes without well-developed accessory process; pleotelsonic boss well-developed, without raised pointed corners 5
5 Apices of bidentate processes swollen, each with short, downwardly-directed spur; pleotelsonic boss plate-like with two forward-facing pegs; body exhibiting various degree of setation, sometimes hirsute (Fig. 2E–F) D. edwardsi
Bidentate processes without swollen apices or spurs, pleotelsonic boss not plate-like 6
6 Pleotelsonic boss comprised of two right-angled triangular structures separated by a deep groove (however, the boss may be very low lying in some specimens, e.g. those from the Black Sea); arms of bidentate process tapering to point, rugose dorsally (Fig. 2J–K) D. bicolor
Pleotelsonic boss comprising two hemispherical structures separated by a wide or a narrow groove, joined at the base 7
7 Pleotelsonic boss large, bilobed, two halves separated by a narrow groove; arms of bidentate process of similar width with along length, dorsally tuberculate (Fig. 2C–D) D. magnitorata
Pleotelsonic boss large, bilobed, two halves separated by a wide v-shaped groove; arms of bidentate process tapering to point, sparsely rugose dorsally (Fig. 2A–B) D. bidentata

Key to pre-ovigerous females (stage 7) and juveniles of Dynamene spp. along the NE Atlantic-Black Sea axis

1 Sphaeromatid without process arising from the posterior margin of the pereonite 6, and with simple pleotelsonic foramen; with or without dorsal tuberculation juvenile and ♀♀ Campecopea , Dynamene and Ischyromene
Without tuberculation on surface of posterior pereonites, pleonites and/or pleotelsonic dome (Figs 1A, B; Figs 4-upper row 6-8, 3A–M) juvenile and ♀♀ Dynamene...2
2 Body flattened, epimera flattened to form a shelf round the body; pleotelsonic foramen at end of a well-developed tube (Fig. 3J-K) D. tubicauda
Body convex, pleura not flattened to form shelf round body; pleotelsonic foramen either flush with edge of pleotelson or at end of a short tube 3
3 Pleotelsonic dome smoothly rounded in side view, pleotelsonic foramen open and flush with edge of pleotelson or at end of short tube 4
Pleotelsonic dome keeled in side view, with or without a median protuberance 5
4 Pleotelsonic foramen open and flush with edge of pleotelson (Fig. 3A–B) D. bidentata
Pleotelsonic foramen at end of short tube (Fig. 3L–M) D. bifida
5 Pleotelsonic dome keeled in side view, pleotelsonic foramen flush with edge of pleotelson Fig. 3C–DD. magnitorata and Fig. 3H, ID. bicolor
Pleotelsonic dome keeled in side view, with median protuberance; pleotelsonic foramen at end of short tube (Fig. 3E, F, G) D. edwardsi

Notes: When identifying Dynamene juveniles and ♀♀ care must be taken not to confuse them with those of Ischyromene lacazei Racovitza, 1908 and Campecopea lusitanica (Nolting, Reboreda & Wägele, 2008). If in doubt, then consult Schüller and Wägele (2005) and Bruce and Holdich (2002) respectively.

Except for size, juveniles are very similar to stage 7 females. Dynamene magnitorata and D. bicolor females are very similar and cannot be keyed out, except on size – on average D. magnitorata tends to be larger (see main text). Ovigerous females are very similar between species and it is not possible to create a key for them. They are characterized by metamorphosed mouthparts, ventral marsupium, wide body and a pleotelsonic foramen that is more upturned and which gradually becomes closed posteriorly (Fig. 4–upper row 8).

Acknowledgments

We acknowledge use of data from the National Biodiversity Network (NBN Gateway database) for Britain and Northern Ireland, in particular those belonging to the Centre for Environmental Data and Recording (CEDaR, Northern Ireland), the Countryside Council for Wales, the Joint Nature Conservation Committee, the Marine Biological Association (DASSH Data Archive Centre), and the Porcupine Marine Natural History Society. Records for Eire were obtained from the National Biodiversity Data Centre (Ireland). We also thank Colin French for permission to use his database (ERICA) containing records for Cornwall and the Isles of Scilly and to David Fenwick Senior for his records and advice.

Much of the material used for this study comes from the private collection of David Holdich, who gives thanks to those below for donating or loaning it to him. All of this material is now deposited in the collection of crustaceans held in the Naturalis Biodiversity Center (Royal Natural History Museum, Leiden, The Netherlands), which already has an extensive collection of Dynamene, and which was also used in this study (see Methods section for catalogue numbers). Thanks are due to Karen van Dorp for incorporating the new material and looking after the collection. In addition, some material that was examined is held in the crustacean collections of the Natural History Museum, London; the Museum of Natural History, Paris and the Portuguese Museum of Natural History and Science, Lisbon.

Thanks are due to following for supplying material to DMH and PV for this study: Anadon R (University of Oviedo, Spain); Atta MM (University of Alexandria, Egypt); Băcescu M (Museum of Natural History, Bucharest, Romania); Costa A (University of the Azores, S. Miguel); Castello J (University of Barcelona, Spain); Ferrario J and Marchini A (University of Pavia, Italy); Fenwick DS Senior (England); Fischelson L (University of Tel Aviv, Israel); Fresi E (Marine Ecological Laboratory, Ischia, Italy); Gönlügür-Demirci G (Ondokuz Mayis University, Turkey); Gözler AM (Rize University, Turkey); Haran T (Tel Aviv University); Jones DA (University of Swansea, Wales); Jones M (University of Plymouth, England); Junoy J (University of Alcalá, Spain); Kirkim F (Ege University, Turkey); Kussakin OG (Far East Science Centre, Vladivostok, Russia); Maggiore F (University of Rome, Italy); McGraff D (University of Galway, Eire); Messana G (University of Florence, Italy), Naturalis Biodiversity Centre (Royal Natural History Museum, Leiden, The Netherlands); Reboreda P (University of Santiago de Compostela, Spain); Schieke U (Marine Ecological Laboratory, Ischia, Italy); Sconfietti R (University of Pavia, Italy); Scott RS (Leicester University, England: Monach Island survey, Scotland); Storey M (England) and Zibrowius H (Endoume Marine Station, Marseilles, France).

The authors also wish to thank the colleagues who helped during fieldwork and sample processing: Tavares M, Cleary D, Santos R, Berecibar E, Ladeiro B, Albuquerque R, Peteiro L and Azevedo CS.

This work is part of the DiverseShores - Testing associations between genetic and community diversity in European rocky shore environments (PTDC/BIA-BIC/114526/2009) research project, funded by the Fundação para a Ciência e Tecnologia (FCT) under the COMPETE programme supported by the European Regional Development Fund. FCT also supported a Ph. D. grant to Pedro Vieira (SFRH/BD/86536/2012).

Thanks are also due to Niel Bruce (Museum of Tropical Queensland, Townsville, Australia) for advice and suggestions, and for reading a draft of the manuscript.

References

  • Adams J (1800) Description of some marine animals found on the coast of Wales. Transactions of the Linnean Society of London 5: 7–13. doi: 10.1111/j.1096-3642.1800.tb00574.x
  • Arrontes J, Anadón R (1990a) Distribution of intertidal isopods in relation to geographical changes in macroalgal cover in the Bay of Biscay. Journal of Marine Biological Association of the United Kingdom 70: 283–293. doi: 10.1017/S0025315400035402
  • Arrontes J (1991) Colour polymorphism in relation to spatial distribution in some intertidal isopods in Northern Spain. Journal of Marine Biological Association of the United Kingdom 71: 749–758. doi: 10.1017/S002531540005342X
  • Bakir AK, Katağan T, Aker HV, Özcan T, Sezgin M, Ateş AS, Koçak C, Kirkim F (2014) The marine arthropods of Turkey. Turkish Journal of Zoology 38: 765–831. doi: 10.3906/zoo-1405-48
  • Barrett J, Yonge C (1964) Collins Pocket Guide to the Sea Shore. Collins, Ammanford, 272 pp.
  • Barrois T (1888) Catalogue des crustacés marins recueillis aux Açores durant les mois d'Août et Septembre 1887. LeBigot frères, Lille, 110 pp.
  • Başçïnar NS, Saǧlam H (2009) Feeding habits of black scorpion fish Scorpaena porcus, in the South-Eastern Black Sea. Turkish Journal of Fisheries and Aquatic Sciences 9: 99–103. http://www.trjfas.org/uploads/pdf_735.pdf
  • Bellan-Santini D (1962) Étude floristique et faunistique de quelques peuplements infralittoral de substrat rocheux. Recueil des Travaux de la Station Marine d’Endoume 50: 249–262.
  • Borg JA, Rowden AA, Attrill MJ, Schembri PJ, Jones MB (2006) Wanted dead or alive: high diversity of macroinvertebrates associated with living and “dead” Posidonia oceanica matte. Marine Biology 149: 667–677. doi: 10.1007/s00227-006-0250-3
  • Borges PAV, Costa A, Cunha R, Gabriel R, Gonçalves V, Martins AF, Melo I, Parente M, Raposeiro P, Rodrigues P, Santos RS, Silva L, Vieira P, Vieira V (Eds) (2010) A List of the Terrestrial and Marine Biota from the Azores. Princípia, Cascais, 430 pp.
  • Bruce NL (1997) A new genus of marine isopod (Crustacea: Flabellifera: Sphaeromatidae) from Australia and the Indo-Pacific region. Memoirs of Museum Victoria 56: 145–234. http://biostor.org/reference/103898
  • Bruce NL, Holdich DM (2002) Revision of the isopod crustacean genus Campecopea (Flabellifera: Sphaeromatidae), with discussion of the phylogenetic significance of dorsal processes. Journal of Marine Biological Association of the United Kingdom 82: 51–58. doi: 10.1017/S0025315402005179
  • Butler E (1878) The natural history of Hastings and St. Leonards and the vicinity. 1st Suppl. United Kingdom.
  • Castelló J (1986) Sobre la fauna de crustáceos isópodos litorales de Cataluña y Baleares. (III). Flabeliifera. Publicaciones del Departamento de Zoología, Universidad de Barcelona 12: 59–69.
  • Castelló J, Carballo JL (2001) Isopod fauna , excluding Epicaridea , from the Strait of Gibraltar and nearby areas (Southern Iberian Peninsula). Scientia Marina 65: 221–241. doi: 10.3989/scimar.2001.65n3221
  • De Grave S, Holmes JMC (1998) The distribution of marine isopods (Crustacea) in Lough Hyne. Biology & Environment, Proceedings of the Royal Irish Academy 98B: 23–30. http://www.jstor.org/stable/20500015
  • Ferraz RR, Santos V, Visión S, Guerreiro G, Carditos F, Frade P, Tempera F, Santos RS (2004) Caracterização ecológica e sócio-económica do sítio de importância comunitária Costa Nordeste e Ponta do Topo (PTJOR0013) e medidas de gestão propostas. Arquivos do DOP (Série Estudos) 20/2004. University of Azores, Department of Oceanography and Fisheries, Azores (Portugal), IV, 57 pp.
  • Galil BS, Marchini A, Occhipinti-Ambrogi A, Minchin D, Narščius A, Ojaveer H, Olenin S (2014) International arrivals: widespread bioinvasions in European Seas. Ethology Ecology & Evolution 26: 2–3, 152–171. doi: 10.1080/03949370.2014.897651
  • Gönlügür-Demirci G, Katağan T (2004) Qualitative and quantitative investigations on Ulva rigida facies from the upper infralittoral zone along Sinop coast, middle Black Sea. In: Ozturk B, Mokievsky VO, Topaloğlu B (Eds) International Workshop on Black Sea Benthos, İstanbul (Turkey), April 2004. Turkish Marine Research Foundation, Istambul, 161–170.
  • Guerra-García JM, Baeza-Rojano E, Cabezas MP, García-Gómez JC (2011) Vertical distribution and seasonality of peracarid crustaceans associated with intertidal macroalgae. Journal of Sea Research 65: 256–264. doi: 10.1016/j.seares.2010.12.001
  • Guerra-García JM, Ros M, Izquierdo D, Soler-Hurtado MM (2012) The invasive Asparagopsis armata versus the native Corallina elongata: differences in associated peracarid assemblages. Journal of Experimental Marine Biology and Ecology 416/417: 121–128. doi: 10.1016/j.jembe.2012.02.018
  • Hansen HJ (1905) On the propagation, structure, and classification of the Family Sphaeromidae. Quartely Journal of Microscopical Science 49: 69–135. http://biostor.org/reference/60090
  • Harrison K (1982) Taxonomy of some Australian serolid and sphaeromatid isopods (Crustacea). PhD Thesis, University of Nottingham, Nottingham.
  • Harrison K, Ellis JP (1991) The genera of the Sphaeromatidae (Crustacea: Isopoda): a key and distribution list. Invertebrate Taxonomy 5: 915–952. doi: 10.1071/IT9910915
  • Harvey CE, Jones MB, Naylor E (1973) Some factors affecting the distribution of estuarine isopods (Crustacea). Estuarine and Coastal Marine Science 1: 113–124. doi: 10.1016/0302-3524(73)90064-9
  • Hayward PJ, Ryland JS (1995) Handbook of the Marine Fauna of North-west Europe. Oxford University Press, Oxford, 816 pp.
  • Hesse M (1873) Mémoire sur des Crustacés rare et nouveaux des côtes de France. Annales des sciences naturelles, Zoologie 5/17: 1–35.
  • Holdich DM (1968a) A systematic revision of the genus Dynamene (Crustacea: Isopoda) with description of three new species. Pubblicazioni Della Stazione Zoologica di Napoli 36: 401–426.
  • Holdich DM (1968b) Reproduction growth and bionomics of Dynamene bidentata (Crustacea - Isopoda). Journal of Zoology 156: 137–153. doi: 10.1111/j.1469-7998.1968.tb05925.x
  • Holdich DM (1968c) The biology of Dynamene bidentata (Adams) and some related sphaeromatid Isopoda. PhD Thesis, University of Wales, Swansea.
  • Holdich DM (1969) Polychromatism in the genus Dynamene (Crustacea: Isopoda). Pubblicazioni Della Stazione Zoologica di Napoli 37: 18–27.
  • Holdich DM (1970) The distribution and habitat preferences of the Afro-European species of Dynamene (Crustacea: Isopoda). Journal of Natural History 4: 419–438. doi: 10.1080/00222937000770401
  • Holdich DM (1971) Changes in physiology, structure and histochemistry occurring during the life-history of the sexually dimorphic isopod Dynamene bidentata (Crustacea: Peracarida). Marine Biology 8: 35–47. doi: 10.1007/BF00349343
  • Holdich DM (1976) A comparison of the ecology and life cycles of two species of littoral isopod. Journal of Experimental Marine Biology and Ecology 24: 133–149. doi: 10.1016/0022-0981(76)90099-X
  • Holdich DM, Harrison K (1980) The isopod genus Dynamene from Australian waters, with description of a new species from coral reefs. Memoirs of Museum Victoria 20: 163–170. http://biostor.org/reference/151868
  • Holthuis LB (1956) Isopoda en Tanaidacea. Fauna van Nederland 16: 1–280.
  • Izquierdo D, Guerra-García JM (2011) Distribution patterns of the peracarid crustaceans associated with the alga Corallina elongata along the intertidal rocky shores of the Iberian Peninsula. Helgoland Marine Research 65: 233–243. doi: 10.1007/s10152-010-0219-y
  • Kirkim F (1998) Ege denizi Isopoda (Crustacea) faunasinin sistematiği ve ekolojisis üzerine araştirmalar. PhD Thesis, Ege Üniversitesi fen Bilimleri Enstitüsü, Izmir.
  • Kussakin OG (1979) [Marine and brackish water isopods of cold and temperate regions of the Northern Hemisphere (including the Black Sea but not the Mediterranean). Part I. Suborder Flabellifera]. Opred Faune SSSR Akad Nauk 122: 1–470.
  • Leach WA (1814) Crustaceology. In ‘Edinburgh Encyclopedia’ 7: 383–347.
  • Ledoyer M (1962) Étude de la faune vagile des herbiers superficiels de Zostéracees et de quelque biotopes d’algues littorales. Recueil des Travaux de la Station Marine d’Endoume (Bull. 25): 117–235.
  • Lucas H (1849) Histoire naturelle des animaux articulés. Exploration scientifiques de l’Algérie pendant les annes 1840, 1841, 1842. Sciences physiques Zoologie I: 1-403. Paris.
  • Maggiore F, Fresi E (1984) Presence of Dynamene bidentata (Adams, 1800) in the Mediterranean (Isopoda). Crustaceana 46: 309–313. doi: 10.1163/156854084X00234
  • Messana G (2004) How can I mate without an appendix masculina? The case of Sphaeroma terebrans Bate, 1866 (Crustacea, Isopoda, Sphaeromatidae). Crustaceana 77: 499–515. doi: 10.1163/1568540041643346
  • Monod T (1923) Fauna de l’appontement de l’administration à Port-Etienne. Bulletin de la Société Zoologique de France 48: 313–316.
  • Monod T (1932) Tanaidaces et Isopodes aquatic de l’Afrique occidentale et septentrionale. Pt3. Sphaeromatidae. Mémoire Société des Sciences Naturelles du Maroc 29: 1–91.
  • Myers P, Espinosa R, Parr CS, Jones T, Hammond GS, Dewey TA (2008) The Animal Diversity. Michigan. http://animaldiversity.org/ [cited 2010 April 29]
  • Moyse J, Nelson-Smith A (1964) Effects of the severe cold of 1962-63 upon shore animals in South Wales. Journal of Animal Ecology 33: 183–190.
  • Omer-Cooper J, Rawson J (1934) Notes on the British Sphaeromatidae (Crustacea, Isopoda). Reports of the Dove Marine Laboratory 3: 22–58.
  • Pauli VL (1954) Free living isopods of the Black Sea. Travaux of the Sevastopol Biological Station 8: 100–135.
  • Pereira SG, Lima FP, Queiroz NC, Ribeiro P, Santos AM (2006) Biogeographic patterns of intertidal macroinvertebrates and their association with macroalgae distribution along the Portuguese coast. Hydrobiologia 555: 185–192. doi: 10.1007/s10750-005-1115-3
  • Picker MD, Griffiths CL (2011) Alien and Invasive Animals – A South African Perspective. Struik-Random House Publishers, Cape Town, 240 pp.
  • Poore GCB, Bruce NL (2012) Global diversity of marine isopods (except asellota and crustacean symbionts). PLoS ONE 7: e43529. doi: 10.1371/journal.pone.0043529
  • Rafrafi-Nouira S, Kamel-Moutalibi O El, Boumaïza M, Reynaud C, Capapé C (2016) Food and feeding habits of black scorpionfish, Scorpaena porcus (Osteichthyes: Scorpaenidae) from the northern coast of Tunisia (Central Mediterranean). Journal of Ichthyology 56: 107–123. doi: 10.1134/S0032945216010112
  • Rathke H (1837) Zur Fauna der Krym. Mémoires of the Academy of Imperial Science, St Petersburg 3: 291–454.
  • Richardson H (1905) Monographs on the Isopods of North America. Govt print off, Washington, 800 pp. doi: 10.5962/bhl.title.1031
  • Rivosecchi ET (1961) Osservazione a Sabellaria di Lavinio. Rendiconti Accademia Nazionale dei XL 12: 147–157.
  • Rodrigues LSB (1990) Estudo dos isópodes (Crustacea: Isopoda) do litoral da ilha das Flores (Açores). Relatórios e Comunicações do Departamento de Biologia 18: 113–115.
  • Schotte M, Kensley B (2005) New species and records of Flabellifera from the Indian Ocean (Crustacea: Peracarida: Isopoda). Journal of Natural History 39(16): 1211–1282. doi: 10.1080/00222930400005757
  • Scott T (1899) Notes on some Crustacea from Granton, Firth of Forth. The Annals of Scottish Natural History 30: 115–116.
  • Schüller M, Wägele JW (2005) Redescription of Ischyromene lacazei Racovitza, 1908 (Isopoda: Sphaeromatidae) from the Mediterranean coast of southern France. Organisms Diversity and Evolution 5[Electr Suppl. 8]: 1–14. doi: 10.1016/j.ode.2004.10.012
  • Tinturier-Hamelin E (1962) Sur le polychromatism de l’Isopode Flabellifère Dynamene bidentata (Adams). I. Premiers resultats d’une étude génétique. Comptes rendus hebdomadaires des séances de l’Académie des Sciences 254: 3906–3908.
  • Tinturier-Hamelin E (1967) Sur le polychromatism de l’Isopode Flabellifère Dynamene bidentata (Adams). II. Étude génétique due mutant bimaculata partiellement lie au sexe. Archives de zoologie expérimentale et générale 108: 511–520.
  • Torelli B (1930) Sferomidi del Golfo di Napoli: revisione degli sferomoidi mediterranei. Pubblicazioni Della Stazione Zoologica di Napoli 10: 297–343.
  • Torrecilla-Roca I, Guerra-García JM (2012) Feeding habits of the peracarid crustaceans associated to the alga Fucus spiralis in Tarifa Island, Cádiz (Southern Spain). Zoologica Baetica 23: 39–47. https://idus.us.es/xmlui/handle/11441/28212
  • Verhoeff E (1944) Sorrentosphaera n.g. (Sphaeromidae) und zur vergleichenden Morphologie der Uropoden. Zoologischer Anzeiger Leipzig 144: 156–162.
  • Viejo RM (1997) The effects of colonization by Sargassum muticum on tidepool macrofauna assemblages. Journal of Marine Biological Association of the United Kingdom 77: 325–340. doi: 10.1017/S0025315400071708
  • Vieira P, Gomes N, Holdich DM, Queiroga H, Costa FO (2015) Phylogeographic structure of Dynamene edwardsi (Crustacea: Isopoda) matches remarkably the sequential genesis of the Macaronesian islands. In: (2015) Scientific abstracts from the 6th International Barcode of Life Conference / Résumés scientifiques du 6e congrès international « Barcode of Life ». Genome 58(5): 163–303. doi: 10.1139/gen-2015-0087