Epimeria (Verheye et al., 2016)

d’Acoz, Cédric d’Udekem & Verheye, Marie L., 2017, Epimeria of the Southern Ocean with notes on their relatives (Crustacea, Amphipoda, Eusiroidea), European Journal of Taxonomy 359, pp. 1-553 : 14-19

Genus Epimeria Costa in Hope, 1851

Gammarellus Herbst, 1793: 106 –115 (in part); type species: Gammarus homari Fabricius, 1779 [currently Gammarellus homari ( Fabricius, 1779) ].

Vertumnus White, 1847: 89 ; type species: Vertumnus cranchii Leach’s manuscript name; nomen nudum.

Vertumnus White, 1850a: 97 [+ pl. 16 figs 3–5 illustrating Leach’s specimens, as Acanthonotus testudo ] (real identity of the specimens: Epimeria cornigera ( Fabricius, 1779) , not Pereionotus testudo (Montagu, 1808)) ; Vertumnus White, 1850 = preoccupied and invalid objective synonym of Epimeria Costa in Hope, 1851 (see remarks below).

Epimeria Costa in Hope, 1851: 24, 46; type species: Epimeria tricristata Costa in Hope, 1851: 46 (= Gammarus corniger Fabricius, 1779: 383 ).

Epimeriella Walker, 1906: 17 ; type species: Epimeriella macronyx Walker, 1906 .

Pseudepimeria Chevreux, 1912: 216 (9 on reprints); type species: Pseudepimeria grandirostris Chevreux, 1912 .

Metepimeria Schellenberg, 1931: 162 ; type species: Metepimeria acanthurus Schellenberg, 1931 .

Subepimeria Bellan-Santini, 1972: 225 ; type species: Subepimeria geodesiae Bellan-Santini, 1972 .

Gammarus – Fabricius 1779: 383 (in part). — H. Milne Edwards 1840: 42–55 (in part).

Vertumnus – White 1850b: 51. — Spence Bate & Westwood 1862: 231. — Norman 1869: 280.

Acanthonotus – White 1850a: 97, pl. 16 figs 3–5; 1850b: 51 (in part); 1857: 177. — Gosse 1855: 139, 142. — Spence Bate 1857: 141; 1862: 120. — Spence Bate & Westwood 1862: 231. — Carus 1885: 410.

Epimeria – Costa 1857: 175, 197; 1867: 42–44 (discussion). — Spence Bate 1862: 153–154. — Boeck 1871: 185 (105 on reprints); 1876: 232. — Stebbing 1888: 877–878 (ubi syn.); 1906: 321. — G.O. Sars 1893: 363 –364. — Holmes 1904: 467: key. — Kunkel 1918: 48 (key). — Stephensen 1928: 253–254; 1929: 130. — Chevreux & Fage 1925: 190–191. — Gurjanova 1951: 666; 1955: 189– 191. — J.L. Barnard 1961: 102; 1969: 394. — McCain 1971: 159. — Karaman & J.L. Barnard 1979: 108 –109. — Lincoln 1979: 434. — Watling & Holman 1980: 642–643. — Moore 1981: 749. — Andres & Lott 1986: 133 (discussion). — Ledoyer 1986: 860; 1993: 616. — J.L. Barnard & Karaman 1991: 380, 393. — Coleman 1998b: 215; 2007: 31. — Wakabara & Serejo 1999: 630– 631. — Lörz & Brandt 2004: 179–190 (phylogeny). — Lörz & Held 2004: 4–15 (phylogeny).

Amphithoë – M. Sars 1859: 130–143 (in part).

Acanthosoma – Boeck 1861: 665–666 (in part); 1869: 410 (in part).

Acanthonotosoma [sic] – Della Valle 1893: 674, in part (ubi syn.).

Metepimeria – Gurjanova 1951: 189; 1955: 189, 209. — J.L. Barnard 1969: 396. — Watling & Holman 1981: 215. — J.L. Barnard & Karaman 1991: 380, 397. — Lörz & Brandt 2004: 184, 188. — Coleman 2007: 61.

Epimeriella – Gurjanova 1955: 189. — J.L. Barnard 1969: 161, 395. — Holman & Watling 1983: 31 (discussion). — Andres & Lott 1986: 131–136. — J.L. Barnard & Karaman 1991: 380, 394, 702. — Coleman 1998b: 215; 2007: 56. — Lörz & Brandt 2004: 179, 184, 188, 189.

Pseudepimeria – Gurjanova 1955: 189, 190. — J.L. Barnard 1969: 396.

non Gammarus Fabricius, 1775: 418 ; type species: Cancer pulex Linnaeus, 1758 . non Acanthonotus Bloch, 1797: 112–114 , pl. 431; type species: Acanthonotus nasus Bloch, 1797 ;

objective synonym of Notacanthus Bloch, 1788: 278 (type species: Notacanthus chemnitzii Bloch,

1788) ( Pisces). non Acanthonotus Cuvier, 1800 : table 4; nomen nudum ( Pisces). non Acanthonotus Goldfuss, 1809: 308 ; objective synonym of Echidna Cuvier, 1797: 143 (Mammalia) . non Acanthonotus Gray, 1830 : pl. 85, fig. 1; type species: Silurus (Acanthonotus) Cuvieri Gray, 1830

(Pisces). non Acanthonotus Swainson & Richardson, 1832: 168 ; nomen nudum ( Aves). non Acanthonotus Ross, 1835 : xc; type species: Acanthonotus cristatus Ross, 1835 . non Ampithöe Leach, 1814: 432 ; type genus: Cancer rubricatus Montagu, 1808 . non Vertumnus Otto, 1823: 294 , pl. 41 fig. 1; type species: Vertumnus thetidicola Otto, 1823 (Trematoda) . non Acanthosoma Curtis, 1824 : unnumbered pagina referring to plate 20 ( Hemiptera ). non Acanthosoma Ross, 1835: 91 ; type species: Acanthosoma hystrix Ross, 1835 . non Acanthonotozoma Boeck, 1876: 237 ; type species: Acanthonotus cristatus Ross, 1835 . non Amphithoë – Latreille 1816: 470 (misspelling for Ampithöe Leach, 1814 ). non Vertumnus – Goës 1866: 522. — Boeck 1871: 99. — Miers 1877: 135. — G.O. Sars 1883: 26 (all

three = Acanthonotozoma ) [unaccepted subjective use of Vertumnus White, 1850 ].

Etymology

“Probably so called from the epimera or side-plates” ( Stebbing 1888: 1672).

Description

Body smooth or covered with teeth or processes. If processes are present on pereionites just above connection with coxae, these processes are small, not sword-like, not forming large longitudinal carinae. Head high; lateral head lobes very reduced; inferior antennal sinus very shallow; ventral lobe of head well developed, oriented obliquely downwards, sharp or rounded. Development of rostrum variable, usually well developed but sometimes small or even tiny. Urosomite 1 always with dorsal process, which can be rounded or tooth like, projecting upwards or backwards. Telson usually distinctly incised or cleft, rarely weakly emarginate or entire, without spines or setae. Eyes usually present, rarely absent (in abyssal species), medium-sized to large, bulging when present, elliptic, pyriform, rounded or reniform, usually with distinct ommatidia. Antenna 1: peduncular articles short or fairly short, with or without teeth; peduncular article 2 shorter than 1 and longer than 3; accessory flagellum present, small, consisting of one article. Mouthparts projecting quadrately. Upper lip almost entire to notched, symmetrical; epistome not very broad. Mandible: incisor ordinary, toothed; lacinia mobilis present on both mandibles (left and right one different), uniplated; setal row present and well-developed; molar process present, large, triturative or not. Lower lip inner lobes absent, outer lobes relatively broad. Maxilla 1 of basic shape, identical on left and right appendage; palp 2-articulate, article 2 with distal marginal row of conical spines and distal marginofacial row of strong setae. Maxilla 2, with plates of basic form; inner plate without facial row of setae. Maxilliped: inner and outer plates large and broad; outer plates reaching about mid of article 2 of palp, with short spines on medial border, with long spines on tip and with long stout setae on distal part of lateral border (the short spines intergrades into long spines which themselves intergrade in long stout setae); inner plates nearly reaching tip of article 1 of palp; palp article 4 usually well developed, but sometimes absent, with distal unguis. Coxae long. Coxae 1–4 progressively longer. Coxae 1–3 narrow. Coxa 4 five-sided: border connecting with coxa, anterodorsal border (running along the posterior margin of coxa 3) perpendicular to body axis or projecting obliquely forward; anteroventral border projecting posteriorly backwards (anterodorsal and anteroventral border either separated by angular discontinuity or smoothly intergrading into a regular curve, rarely produced into a tooth); posteroventral border straight or concave, separated from anteroventral border by angle or tooth (ventral angle or tooth); posterodorsal border concave, separate from posteroventral border by a tooth (posterior tooth); a carina or a groove often run on the surface separating ventral and posterior teeth/angles; when present this carina sometimes bear a tooth projecting laterally. Coxae 5–6 with or without tooth or process projecting laterally; when coxa 5 laterally dentate, its tooth can be very large. Gnathopods weak, usually similar but never identical; gnathopod 2 always longer than gnathopod 1 (usually just a bit longer, but sometimes distinctly longer); gnathopods usually subchelate, but sometimes simple; carpus and propodus short to very long, and robust to very narrow; palm well defined or not (sometimes absent), usually posteriorly with about 3 long spines; posterior border of dactylus dentate (sometimes strongly dentate), with terminal unguis. Pereiopods 3–7 with terminal unguis on dactylus, easily breaking at the merocarpal articulation. Pereiopod 6> pereiopod 5> pereiopod 7; basis of pereiopods 5–7 with longitudinal carina on both side, which is often very protruding; dactylus of pereiopods 5–7 usually short, rarely long. Coxal gill from gnathopod 2 to pereiopod 7. Oostegite large and broad, from gnathopod 2 to pereiopod 6. Uropods well developed; rami sword-like. In uropods 1–2, inner ramus slightly longer than outer ramus, slightly shorter than peduncle; tip of rami tapering to form a narrow point without spines (i.e., it is not senticaudate); peduncles without ventrolateral spines. In uropod 3, rami subequal much longer than peduncle, which is very short; outer ramus entire.

Body length

8 to 80 mm.

Distribution and biology

The genus Epimeria is almost cosmopolitan in distribution, reaching its highest diversity in Antarctic seas. It also comprises a fairly large number of tropical, deep-water Indo-Pacific species, for which the largest part remains undescribed (pers. obs.: samples from the Muséum national d’Histoire naturelle, Paris). Epimeria has been recorded from the intertidal ( E. monodon Stephensen, 1947 ) down to 5695 m ( E. abyssalis Shimomura & Tomikawa 2016 — see Shimomura & Tomikawa (2016)), but it is predominantly found between 150 and 2500 m. No shallow-water records are known from tropical and warm-temperate seas. The majority of Epimeria species are slow moving, strictly benthic amphipods ( Dauby et al. 2001a) but they are able to swim quickly over short distances ( Moore 1981). At least two highly modified species are truly pelagic: E. macronyx ( Walker, 1906) and E. pelagica ( Birstein & Vinogradov, 1958) , and a few species, including E.scabrosa (K.H. Barnard, 1930) and E.atalanta sp. nov., are suspected by us to be semi-pelagic, as they are poorly calcified and exhibit a gracile morphology. Epimeria are usually associated with communities rich in epifauna ( De Broyer et al. 2001). The material examined for this study shows that the diversity of Epimeria is directly proportional to the abundance of erect epifauna in trawl catches. The shallow-water species Epimeria monodon lives amidst macro-algae ( Richardson 1977). Most species are carnivorous and feed on a fairly large range of organisms, albeit with individual preferences for each species ( Dauby et al. 2001a). One European species, Epimeria parasitica (M. Sars, 1859) , is an ectoparasite of holothurians (M. Sars 1859). Epimeria species are themselves frequently consumed by fishes (e.g., Olaso et al. 2000; Dauby et al. 2003). Females largely predominate in the catches. Different hypotheses may be advanced as possible explanation: differences in behavioural pattern between males and females, a smaller size and/or shorter lifespan in males, a biased sex ratio, or even protandrous hermaphroditism. Epimeria seem to be iteroparous, at least in some cases. Indeed, within the maxilliped of the specimen of Epimeria (Drakepimeria) sp. 1 dissected by M. Verheye, which was a mature female with fully developed and setigerous oostegites, the outline of a new cuticle bordered with spines and setae in development could be observed. This indicates that the specimen was preparing an extra moult, after a presumably fertile intermoult. Klages (1991) observed that hatchlings of “ Epimeria georgiana ” (possibly E. xesta ), E. robustoides (under the name E. robusta ) and E. rubrieques climb on the back of their mother and remain there for a short period of time before leaving her. In contrast, he observed that juvenile “ E. macrodonta ” and “ E. similis ” leave their mother immediately after hatching. Cryptoniscin epicaridean isopods have been reported to parasitize Epimeria robusta (see K.H. Barnard 1930), E. robustoides (see Klages 1991, as E. robusta ) and E. rubrieques (see Klages 1991). According to K.H. Barnard (1930), the parasites occupy the marsupium of the female.

Remarks

The body of many Epimeria species is adorned with protrusions, crests or teeth, which can sometimes be very high. Two main conjectural explanations have been previously proposed to explain the role of the dentiform processes in Epimeria and other amphipods: defence against predation ( Moore 1981; Brandt 2000) and hydrodynamic stabilizers during swimming ( Moore 1981). However the second explanation seems less applicable for most Epimeria , which are benthic and swim only for short distances ( Moore 1981). We herein propose a third explanation, that ornamentation might play a role of camouflage, specifically disruptive camouflage. This idea is based on the analogous observations of the first author for a tuberculate pleustid Pleustes panoplus (Kröyer, 1838) [an eusiroid amphipod species superficially similar to Epimeria ] on a rocky shore near Tromsø ( Norway). Their protuberances, combined with a variegated colouration, made individuals almost perfectly blend with their habitat of rocks covered in epiflora and epifauna. The protrusions of some Epimeria species might constitute a form of disruptive camouflage on substrates rich in epifauna, which are their preferential habitat. As they live at depths, where the light intensity is very low or absent, a perfect camouflage might not be necessary to avoid detection by predators like fishes. A disruptive body form in a complex tridimensional epifaunal environment could efficiently protect them from predation.

The genus Epimeria includes 84 described species (59 in the Southern Ocean). For practical reasons, Antarctic Epimeria species are distributed herein into different subgenera, presenting a homogeneous combination of morphological characters. These subgenera are clades (see Verheye et al. 2016a) or putative clades (their monophyly was assumed from morphological data when some species could not be sequenced). However, the monophyly of the subgenus Urepimeria remains conjectural, since only one of its three species has been sequenced and the morphology of these species is not fully congruent.

The name Vertumnus requires discussion. This generic name was first introduced by Otto (1823) for a trematod: Vertumnus thetidicola Otto, 1823 , for which Otto (1823) gave a detailed description. The name Vertumnus was then introduced a second time by White (1847), as a nomen nudum, based on a manuscript of W.E. Leach about crustaceans. Later, White (1850a) illustrated Leach’s specimens, describing them briefly as ‘ Vertumnus Cranchii ’. These specimens correspond with the description of Epimeria cornigera ( Fabricius, 1779) . However, White (1850a) erroneously considered Vertumnus Cranchii as a junior synonym of Oniscus testudo Montagu, 1808 [currently Pereionotus testudo (Montagu, 1808) ] and used the combination Acanthonotus testudo for it in his text and on the caption of his plate. Thus, it is clear that Epimeria Costa in Hope, 1851 and Vertumnus White, 1850 are synonyms and have the same type species. However, as indicated above, the name Vertumnus White, 1850 is preoccupied by Vertumnus Otto, 1823 . Furthermore, it is unavailable in application of Article 11.6 of the International Code of Zoological Nomenclature ( ICZN 1999), which states: “a name which when first published in an available work was treated as a junior synonym of a name then used as valid is not thereby made available.” The confusion between Oniscus testudo and Epimeria cornigera was repeated by Gosse (1855), who used again the name Acanthonotus testudo for Epimeria cornigera .

A sub-generic classification of non-Antarctic and non sub-Antarctic Epimeria falls out of the scope of the present paper, as these extralimital species form a clade distinct from the Antarctic Epimeria clade ( Verheye et al. 2017). We simply propose a provisional definition of the type subgenus Epimeria , which occurs in the Atlantic, Arctic and Indian Oceans, and in the Mediterranean Sea.

Key to the Antarctic and sub-Antarctic subgenera of Epimeria

1. Rostrum small to large (reaching at least mid of article 1 of peduncle of antenna 1); robust species with tegument normally to strongly calcified ………………………………………2

– Rostrum minute (not reaching 0.2 of article 1 of peduncle of antenna 1), reduced to a tiny blade separating the base of the first article of the peduncles of antennae 1; fragile species with very thin tegument ………………………………………………………………… Epimeriella Walker, 1906

2. Some or all pereionites may have a pair of dorsolateral teeth or protrusions, but they are always devoid of a pair of ventrolateral protrusions or teeth; eyes bulging but not conical; gnathopods not reduced in size, achelate or subchelate; pereiopods 3–7 with merus, carpus and propodus slender to moderately stout, with dactylus normal-sized or long and slender, not folding on propodus …………3

– Pereionites both with pair of dorsolateral teeth or protrusions and with pair of ventrolateral protrusions or teeth (just above coxae); eyes conical; gnathopods very small and achelate; pereiopods 3–7 with merus, carpus and propodus extremely stout and dactylus fairly long, stout, curved and folding on propodus [all pereionites and pleonites with mid-dorsal crest or tooth] ……………………………........………………………… Pseudepimeria Chevreux, 1912

3. Pleonites 2–3 with or 0–2 pairs of dorsolateral protrusions or teeth; when they are two, one is disposed just above the other (and not anteriorly to the other) …………………………………………4

– Pleonites 2–3 with at least 2 pairs of low dorsolateral protrusions, teeth or keels, of which at least two are disposed in longitudinal arrangement [propodus of gnathopods 1–2 fairly slender; pleosomites and posterior pereionites with low mid-dorsal crest] ………………… Metepimeria Schellenberg, 1931

4. Basis of pereiopod 7 broad in all its length, with posterior border not excavated in its distal half; posterior border of basis of pereiopods 5–6 without proximal tooth directed in the same axis as basis (but a proximal rounded lobe projecting laterally can be present) …………………5

– Basis of pereiopod 7 narrow with straight posterior border ( E. heldi ), or basis 7 with posterior border proximally broad and slightly or strongly excavated in its distal half (distal half narrow with posterodistal lobe reduced); posterior border of basis of pereiopods 5–6 with or without proximal tooth directed in the same axis as basis [gnathopods 1–2 subchelate with palm very robust and often expanding distally] ……………………………… Hoplepimeria subgen. nov

6. Some or all pereionites and pleonites 1–2 with LARGE acute-tipped and laterally compressed middorsal tooth; pleonites and some or all pereionites with one (sometimes two) pair(s) of distinct dorsolateral teeth or carinae …………………………………… Drakepimeria subgen. nov.

– Pereionite 7 and pleonites 1–2 with or without SMALL posterordorsal tooth; pleonites and pereionites without dorsolateral teeth or carinae; pereionites 1–6 without ornamentation …………..7

7. Pereionite 7 and pleonites 1–2 without posterodorsal tooth ………………………………………8

– Pleonite 2 with posterodorsal tooth; pleonite 1 and pereionite 7 with or without posterodorsal tooth ………………………………………………………………….. Subepimeria Bellan-Santini, 1972

8. Teeth of the dactylus of gnathopods especially long; mandible with molar process drawn out, without triturative surface; lower lip with wide hypopharyngal gap; pleonite 3 posterodorsally rounded, at most scarcely produced into a lobe; rostrum about 0.5 × as long as article 1 of peduncle of antenna 1 ………………….........................……………… Laevepimeria subgen. nov.

– Teeth of the dactylus of the gnathopods normally developed; mandible with molar process normal, triturative; Lower lip with narrow (V-shaped) hypopharyngeal gap; pleonite 3 posterodorsally produced into a large and strong triangular tooth or into a blunt lobe; rostrum 0.5–1.1 × as long as article 1 of peduncle of antenna 1 ………………………… Urepimeria subgen. nov. *

* Without dissection, Epimeria (Urepimeria) annabellae Coleman, 1994 and E. (U.) monodon Stephensen, 1947 can be readily separated from E. ( Laevepimeria ) spp. by the strong posterodorsal process of their pleonite 3. The pleonite 3 of E. (U.) extensa Andres, 1985 is much less produced and at first glance, the species looks fairly similar to Laevepimeria , if the mouthparts are not examined. However, E. (U.) extensa can easily be identified by its rostrum, which is about 1.1 × as long as article 1 of peduncle of antenna 1. It is about 0.5 × as long as article 1 in Laevepimeria spp.