Eurythenes S.I. Smith

D’Acoz, Cédric D’Udekem & Havermans, Charlotte, 2015, Contribution to the systematics of the genus Eurythenes S. I. Smith in Scudder, 1882 (Crustacea: Amphipoda: Lysianassoidea: Eurytheneidae), Zootaxa 3971 (1), pp. 1-80 : 6-9

Genus Eurythenes S.I. Smith in Scudder, 1882

Eurytenes Lilljeborg, 1865a: 11 (non Eurytenes Förster, 1862 , Hymenoptera ); 1865b: 6. Type species: Lysianassa magellanica H. Milne Edwards, 1848 ; by original designation.

Eurythenes S.I. Smith in Scudder, 1882: 135 (Supplemental list of genera in Zoölogy), 122 (Universal index to genera in Zoölogy).— S.I. Smith, 1884a: 54.— Stoddart & Lowry, 2004: 428 (ubi syn.). Type species: Lysianassa magellanica H. Milne Edwards, 1848 (nom. nov. for Eurytenes Lilljeborg, 1865 ).

Eurysthenes S.I. Smith, 1884b: 181 . Type species: Lysianassa magellanica H. Milne Edwards, 1848 (probable typographical error for Eurythenes S.I. Smith in Scudder, 1882).

Euryporeia G.O. Sars, 1891: 85 . Type species: Lysianassa magellanica H. Milne Edwards, 1848 (nom. nov. for Eurytenes Lilljeborg, 1865 ).

Katius Chevreux, 1905: 1 (type species: Katius obesus Chevreux, 1905 ).

Etymology. Lilljeborg (1965a) indicated the following etymology of Eurytenes : 'On account of its extensive geographical distribution, we give to this genus the name Eurytenes , from the Greek 'εύρυτεής, which signifies widely stretched'.

Description. See description of family Eurytheneidae by Stoddart & Lowry (2004).

Composition. In the present paper, seven Eurythenes species are recognized: E. andhakarae sp. nov., E. gryllus ( Lichtenstein in Mandt, 1822), E. magellanicus (H. Milne Edwards, 1848) , E. maldoror sp. nov., E. obesus ( Chevreux, 1905) , E. sigmiferus sp. nov., and E. thurstoni Stoddart & Lowry, 2004 . DNA sequences of specimens not directly examined and morphological observations published in literature are indicative of the existence of further species.

Nomenclature issues. The name Eurythenes was erected in very unusual manner, and has been a source of confusion for more than a century. Lilljeborg (1865a) created the genus Eurytenes (without "h") for Lysianassa magellanica H. Milne Edwards, 1848 (currently Eurythenes magellanicus ) but this name was preoccupied by Eurytenes Förster, 1862 (Hymenoptera) . On page 135 of the first part of the book by Scudder (1882) (Supplemental list of genera in Zoölogy), ' Eurythenes Lilljeborg. Nova Acta Soc. Sc. Upsal., vii, p. 11. 1865. Crust., Amph. Smith.' is listed. Column 3 of page 122 of the second part of Scudder (1882) (Universal index to genera in Zoölogy) lists ' Eurytenes Först., Hym. 1862 M.' and two lines below ' Eurythenes Lillj. Crust. 1865 . S.' Chevreux (1889) made the following statement (freely translated from French): 'Since Eurytenes was used by Förster for a new genus of Hymenoptera, Smith has slightly modified the spelling of the name proposed by Lilljeborg (1865), so that it remains phonetically identical. In this paper, I keep that spelling of Smith, although I consider the procedure which he followed highly inappropriate'. G.O. Sars (1891) proposed the name Euryporeia G.O. Sars, 1891 as a replacement name for Eurytenes Lilljeborg, 1865 , with the following justification: 'In 1865 Prof. Lilljeborg established this genus to include the remarkable gigantic form described by Milne Edwards under the name of Lysianassa magellanica . The denomination Eurytenes proposed by him having, however, been before adopted for a genus of Hymenoptera , I have changed the latter half of the compound, still conserving the signification of the name as intended by Prof. Lilljeborg.' Fifteen years later, in his classical revision of gammaridean amphipods, Stebbing (1906) implicitly treated Eurythenes S.I. Smith, 1882 as a replacement name validly introduced for Eurytenes Lilljeborg, 1865 . Between 1893 and 1925, a few authors adopted Euryporeia (see the list given by Stoddart & Lowry 2004), but otherwise the point of view of Stebbing (1906) became prevalent and, after 1925, universally accepted. The listing of both ' Eurytenes Först. ' and ' Eurythenes Lillj. ' in the second part of the book of Scudder (1882), which was overlooked by previous authors, clearly indicates that the spelling modification was deliberate and was intended to be a replacement name sensu ICZN (1999) Art. 60.3. As the change operated by Smith has been done within a book authored by Scudder and not by him, it seems advisable to indicate the authority of the genus Eurythenes as 'Smith in Scudder, 1882' and not simply as ' Smith, 1882 ' as it is usually the case.

The name Eurysthenes S.I. Smith, 1884b has been interpreted as a typographical error ( Stoddart & Lowry 2004), since the paper of S.I. Smith (1884b) is a reprint of S.I. Smith (1884a), where the spelling Eurythenes is used.

Biology. Eurythenes obesus is a pelagic species, of which the biology is poorly known, whilst other Eurythenes species are benthopelagic, E. thurstoni being more confined to the pelagic realm than the species of the E. gryllus - complex or E. gryllus s.l. ( Stoddart & Lowry 2004). A substantial corpus of biological literature exists for this species complex. It has to be reviewed collectively because the pseudocyptic species described herein have not been previously separated, assuming that their overall biology is reasonably similar.

Barnard (1962) stated that, "morphologically, E. gryllus s.l. is more pelagic than benthic, but obviously feeds on the bottom”, but Bowman & Manning (1972) found that “the heavy compact body seems poorly adapted for a continuous pelagic existence, even though the heavily muscled pleon indicates that E. gryllus is a strong swimmer". Subsequent papers repeatedly confirmed that E. gryllus s.l. is a benthopelagic species and Thurston (1990) gave an extensive list of papers recording E. gryllus s.l. in the water column, often far above the abyssal sea floor. An extreme case is the record 1800 m above the bottom by Baldwin & Smith (1987). According to observations in the European Basin by Christiansen et al. (1990), it is predominantly found in the first 15 m above the sea floor; juveniles and large females being exclusively found in the first 50 m above the bottom; adult males have a bimodal distribution with maxima at 15 and 300 m above the bottom; isolated specimens were observed 1000 m above the sea floor. Baldwin & Smith (1987), who made fairly similar observations on populations from the central and eastern North Pacific, suspected that juvenile Eurythenes remain close to the bottom due to larger food supplies and the possibility to seek refuge in the sediment as a protection from predation. Concerning pelagic specimens, Ingram & Hessler (1983) state that: "The bathymetric distribution of E. gryllus implies that individuals probably spend long periods above the sediment searching for food. Those that live hundreds of meters above the sediment might only rarely, if ever, descend to the sediment. Such behavior would be energetically expensive unless E. gryllus were neutrally buoyant or nearly so. Their primary energy store, lipids, may aid in maintaining the neutral buoyancy that would require little if any energy expenditure for staying in the water column."

The data of Baldwin & Smith (1987) suggest that Eurythenes gryllus s.l. has a continuous recruitment, as there is no size class progression along with the annual cycle. Hatchlings are 11 mm long ( Thurston & Bett 1995) and according to Ingram & Hessler (1987), in E. gryllus s.l. from the central North Pacific, males mature at instar VIII (mean length 70 mm) and females at instar XV (mean length 109 mm); both males and females are mature through several instars and females can have multiple broods; they estimate that females mature at 9 years and males at 4 years. However, according to Thurston & Bett (1995) the relationship between the size and the instars as calculated by Ingram & Hessler (1987) requires minor adjustments. Adult females with setose oostegites are uncommonly recorded and have very soft teguments compared to males and females in non-brooding intermoult ( Ingram & Hessler 1987, Thurston & Bett 1995). The only brooding female ever caught (bearing hatchlings, not eggs) was caught with a midwater trawl 1500 m above the seafloor, suggesting pelagic incubation, at a depth range where predators are scarce ( Thurston & Bett 1995). We hypothesise that soft (i.e. lighter) teguments would ensure a better buoyancy—hence a reduced energetic budget—during the presumably non-feeding pelagic brooding stage and that females descend to the bottom for releasing their hatchlings.

Eurythenes spp. enter baited traps in swarms (e.g. Shulenberger & Hessler 1974, Premke et al. 2003) and Dauby et al. (2001) considered E. gryllus s.l. to be an exclusive scavenger. However, it has also been shown to predate on fishes caught by long lines ( Templeman 1967) and to ingest mud ( Barnard 1962). Anatomical studies of E. gryllus s.l. have revealed well-developed chemosensory organs on the antennae ( Dahl, 1979), mandibles welladapted for rapidly devouring pieces of carrion ( Thurston 1979, Dahl, 1979) and a midgut capable of storing a large amount of food, as the fall of carcasses is sporadic ( Dahl, 1979). According to Smith & Baldwin (1984), the short range detection of carrion by Eurythenes gryllus s.l. would obviously result from chemoreception, but they suspect that the noise and vibrations of their feeding and swimming would then attract specimens located beyond the odour boundary. Subsequent authors (e.g. Premke et al. 2003) only retained chemoreception and no longer consider the acoustic/vibratory hypothesis. Ingram & Hessler (1983) think that E. gryllus s.l. are hovering above the bottom, like vultures, in order to survey a larger area increasing the probability of detecting odour diffusion plumes of carcasses. E. gryllus s.l. is known to reach carcasses quickly and it has been reported that up to 618 specimens have been caught in a trap, only 12 minutes after its deposition on the sea floor ( Premke et al. 2003). This is however an exceptional case and the arrival of E gryllus s.l. usually takes a longer time ( Thurston 1979). Brooding females of E. gryllus s.l. have so far never entered a trap ( Ingram & Hessler 1983, Charmasson & Calmet 1987).

On several occasions, Eurythenes gryllus s.l. has been found in the stomach of flying sea birds ( Lichtenstein in Mandt 1822; Stephensen 1925, 1949; Chevreux 1935; Ainley et al. 1986; Klages & Cooper 1997). Since these sea birds are obviously unable to dive at the minimal depths were living specimens have been recorded (i.e. below 500 m), it has been suggested that dead Eurythenes would drift towards the surface, where birds would consume them ( Bowman & Manning 1972, Ingram & Hessler 1983). This statement remains however purely speculative. If dead Eurythenes would be drifting towards the surface, they should occasionally wash ashore, which, as far we know, is not corroborated by any records. Ainley et al. (1986) record E. gryllus s.l. in bird stomachs only where pack ice is present and conclude that they presumably occur near the surface level in such environments.

Sexual dimorphism, allometry, individual variations. In Eurythenes there is almost no sexual dimorphism, except for antenna 2, which increases considerably in length in males that reach sexual maturity. The number of setae on the inner plate of maxilla 1 increases with size. The propodus of gnathopod 2 lengthens slightly when specimens increase in size (but the proportions of that article is also partly species-dependent). The spines and setae of pereopods 3–7 and uropods drastically shorten and widen when specimens increase in size. The propodus of pereopods 5–7 becomes slightly longer and narrower when size increases. The number of spines on the anterior border of the propodus of pereopods 5–7 increases with body size. The acuity of the posteroventral tooth of the first and second epimeral plate reduces when size increases. In some species, small specimens (<50 mm) have or may have a posteroventral tooth on the third epimeral plate. This tooth disappears when the specimens get larger. The proportions of coxae and appendages also change with size, albeit very slightly. The rami of uropod 3 widen in large specimens. Finally, in E. magellanicus , some individual variations were observed in the size of the palm of gnathopod 1, the shape of coxa 4 and the strength of crenulation of the posterior basis of pereopods 5–7.

In agreement with literature data on Eurythenes gryllus s.l. (e.g. Smith & Baldwin 1984, Baldwin & Smith 1987, Thoen et al. 2011), we observed that the colour pattern of Eurythenes of the same species (in our case E. andhakarae sp. nov. and E. gryllus s.s.) is extremely variable and may range from white to yellow, orange and red. Baldwin & Smith (1987) propose the following links: (1) pigmentation deposition in animals with increasing length of intermoult period and (2) lower food supply resulting in a longer intermoult period, therefore allowing an increased time to incorporate pigments. This idea of a correlation between the colour and the moult/intermoult cycle is supported by observations on the green shore crab, Carcinus maenas (Linnaeus, 1758) , where only specimens in long intermoult get a red ventral colour ( Reid et al. 1997, Styrishave et al. 2004, Lewis 2011).

Interspecific differences. E. obesus exhibits profound differences with other Eurythenes species. Especially the very long dactylus of its pereopods 3–7 allows for an immediate distinction from all other Eurythenes species. Its ventrally deeply convex coxa 4 and the very elongate shape of its eyes are also very characteristic. E. thurstoni exhibit clear-cut, albeit much less pronounced, differences from the remaining Eurythenes species. Especially, the palm of gnathopod 2 is considerably more protruding than in gryllus and its relatives, the ventral border of its coxa 4 is more rounded and the postero-distal border of the basis of its pereopod 7 is much more elongated than in the remaining species.

A group of extremely similar species remained to be studied, which can be referred as the gryllus -complex. Bowman & Manning (1972) and Stoddart & Lowry (2004) observed and illustrated minute differences between specimens of different origins but considered them as insufficient to justify the recognition of different species. On the other hand, Ingram & Hessler (1983), who also observed differences, did not rule out that they might be of specific nature, but did not investigate the problem in any detail. Molecular data definitely settles the issue and indicates beyond doubt that E. gryllus s.l. consists of several species-level clades ( Havermans et al. 2013). Hence, it was necessary to reconsider the question by a morphological comparison of the different molecular clades and to re-consider the elusive characters previously considered as intraspecific variation, which is commonly referred to as the reverse taxonomy approach (e.g. Kanzaki et al. 2012). Indeed, with the exception of shape of coxa 2 which is markedly different in E. maldoror sp. nov. compared to all other species, other differences are rather difficult to appreciate and should be used with the greatest caution, when trying to identify specimens. Specific characters in the gryllus -complex include:

- degree of carination of body segments and the number of body segments with a sigmoid profile (i.e. with a slight anterior concavity)

- shape of the eyes

- development of the anterior lobe of head

- width and shape of article 2 of the mandibular palp

- number of nodular spines on the anterior border of the inner plate of the maxilliped

- degree of protrusion of the aforementioned nodular spines

- ratio length/width of the basis of gnathopod 1

- degree of protrusion of the palm of gnathopod 1

- shape of the ventral border of coxa 2

- proportions of the propodus of gnathopod 2 (this character is also partly allometric)

- level of protrusion or intrusion of the palm of gnathopod 2

- number of spines defining the palm of gnathopod 2

- proportions and shape of coxa 4 (difficult to phrase in simple and unambiguous terms)

- degree of posterior expansion of the basis of pereopod 7 (and its shape)

- degree of development and shape of the posterodistal lobe of the basis of pereopod 7

- degree of crenulation of the posterior border of the basis of pereopods 5–7 (in keeping in mind that the crenulation is usually more developed in immatures than in adults and that the posterior border of the basis is fragile and hence easily eroded)

- degree of broadening of the merus of pereopod 5–7 (and to a certain extent its shape)

- presence/absence of a posteroventral tooth on the third epimeral plate in specimens <50 mm

- degree of curvature of the ventral border of the third epimeral plate.